- Email: [email protected]
Trace element levels of mushroom species from East Black Sea region of Turkey
Food Control 18 (2007) 806–810 www.elsevier.com/locate/foodcont
Trace element levels of mushroom species from East Black Sea region of Turkey Mustafa Tuzen a, Ertugrul Sesli b, Mustafa Soylak b
c,*
a Gaziosmanpasa University, Faculty of Science and Arts, Department of Chemistry, 60250 Tokat, Turkey Karadeniz Technical University, Faculty of Fatih Education, Department of Biological Education, 61335 So¨gutlu, Trabzon, Turkey c Erciyes University, Faculty of Art and Science, Department of Chemistry, 38039 Kayseri, Turkey
Received 17 November 2005; received in revised form 5 April 2006; accepted 10 April 2006
Abstract The levels of trace metals of mushroom samples collected from East Black Sea region of Turkey were determined by flame and graphite furnace atomic absorption spectrometry after microwave digestion method. The accuracy of the method was corrected by standard reference material (NIST SRM 1573a Tomato Leaves). The contents of investigated trace metals in mushroom samples were found to be in the range of 18.9–64.8 lg/g for copper, 53.5–130 lg/g for manganese, 44.7–198 lg/g for zinc, 187–985 lg/g for iron, 0.54–10.8 lg/g for selenium and 0.9–2.5 lg/g for cadmium. Mushrooms species in the highest levels of trace elements were found Entoloma sinuatum for Cu and Zn, Leucoagaricus leucothites for Mn, Amanita pantherina for Fe and Se, Agaricus arvensis for Cd. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Trace elements; Mushroom; Atomic absorption spectrometry; East Black Sea region – Turkey
1. Introduction The consumption of wild edible mushrooms is increasing, even in the developed world, due to a good content of proteins as well as a higher content of trace minerals (Agrahar-Murugkar & Subbulakshmi, 2005). Wild mushrooms are a popular food source in Turkey. Mushrooms have along history of use in traditional Chinese medicine. Mushrooms have also been reported as therapeutic foods, useful in preventing diseases such as hypertension, hypercholesterolemia, and cancer. These functional characteristics are mainly due to their chemical composition (Manzi, Aguzzi, & Pizzoferrato, 2001). Due to positive and negative effects and the toxicity of heavy metals on both human health and the environment, many researchers are interested in the analysis of trace metal contents of environmental samples and *
Corresponding author. Tel./fax: +90 352 4374933. E-mail addresses: [email protected] (M. Tuzen), soylak@erciyes. edu.tr (M. Soylak). 0956-7135/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2006.04.003
especially foods (Orak, Altun, & Ercag, 2005; Radwan & Salama, 2006; Soylak, Colak, Tuzen, Turkoglu, & Elci, 2006). Accurate and adequate food composition data are invaluable for estimating the adequacy of intakes of essential nutrients and assessing exposure risks from intake of toxic non-essential heavy metals (Onianwa, Adeyemo, Idowu, & Ogabiela, 2001; Soylak, Karatepe, Elci, & Dogan, 2003). Turkey can be separated into seven geographic regions. One of them is the Black Sea region. The Black Sea region can be separated into three smaller geographic regions. The East Black Sea region is one of them. In this region, the climate is mild and rainy. The seasons are normally wet with mild temperatures. The climate during the year, especially, in spring and autumn, is ideal for mushroom growth (Sesli & Tuzen, 1999). In the present study, the contents of selenium, cadmium, iron, copper, manganese and zinc in mushroom samples collected from East Black Sea region of Turkey were determined by flame and/or graphite furnace atomic absorption spectrometry after microwave digestion.
M. Tuzen et al. / Food Control 18 (2007) 806–810
2. Materials and methods Forty eight samples including 16 different mushroom species were collected during field trips in different localities of East Black Sea region of Turkey in 2004. Main ecological and morphological properties of mushroom were noted at the field. The specimens were examined in the laboratory at an earliest convenient time after collection. All the spore measurements were calculated from at least 20 individual measurements using research microscopes. Excised pieces of mushroom were moistened by addition of a few drops of Clemencon’s solution [20 ml concentrated ammonia + 1 g glycerine + 80 ml 96% ethanol] and then sectioned. The fungi (Table 1) were identified according to Breitenbach and Kra¨nzlin (1986, 1991, 1995, 2000). Some specimens were deposited at the personal fungarium of Faculty of Fatih Education at Karadeniz Technical University in Trabzon Province of Turkey. The samples were dried at 105 °C for 24 h for chemical investigations. Dried samples were homogenized using an agate homogenizer and stored in polyethylene bottles until analysis. All the plastic and glassware were cleaned by soaking with the contact overnight in a 10% nitric acid solution and then rinsed with deionized water. One gram of sample was digested with 6 ml of concentrated HNO3 (Suprapure, Merck) and 2 ml of concentrated H2O2 (Suprapure, Merck) in Milestone Ethos D model microwave digestion system (maximum pressure 1450 psi and maximum temperature 300 °C) and diluted to 10 ml with double deionized water (Milli-Q Millipore 18.2 MX cm 1 resistivity). A blank digest was carried out in the same way (digestion conditions for microwave system were applied as 2 min for 250 W, 2 min for 0 W, 6 min for 250 W, 5 min for 400 W, 8 min for 550 W, vent: 8 min, respectively). The accuracy of the method was verified by standard reference materials (NIST SRM 1573a Tomato Leaves). A Perkin–Elmer Analyst 700 model atomic absorption spectrometer with deuterium background cor-
807
rector was used in this study. Selenium and cadmium levels in the mushroom samples were determined by HGA graphite furnace using argon as inert gas. The other elements were determined in air–acetylene flame. 3. Results and discussion Detection limit is defined as the concentration corresponding to three times the standard deviation of ten blanks. Detection limit values of elements as milligram per liter in flame AAS were found to be 0.005 for Cu, 0.010 for Zn, 0.008 for Fe, 0.009 for Mn. Selenium and cadmium were below detection limit of flame AAS. Se and Cd were determined using graphite furnace AAS. The recovery values were nearly quantitative for microwave digestion method. The relative standard deviations were less than 10% for all investigated elements. T-test was used in this study (p < 0.05). The accuracy of the method was evaluated by means of trace metals determination in standard reference material (SRM). The achieved results were in good agreement with certified values. The results for this study are given in Table 2. Trace metal levels in the analysed samples are listed in Table 3. All metal concentrations were determined on a dry weight basis. The concentrations of investigated trace metals in mushroom samples were found to be in the range of 18.9–64.8 lg/g for copper, 53.5–130 lg/g for manganese, Table 2 Observed and certified values of trace metals in NIST SRM 1573a Tomato Leaves, N = 4 Element
Certified value (lg/g)
Our value (lg/g)
Recovery (%)
Cu Zn Mn Fe Se Cd
4.7 30.9 246 368 0.054 1.52
4.64 ± 0.25 29.5 ± 1.9 238.9 ± 13.3 361.5 ± 25.3 0.052 ± 0.004 1.53 ± 0.10
99 95 97 98 96 101
Table 1 Habitat, edibility and names of mushrooms No
Fungarium
Name of mushroom
Habitat
Edibility
Family
01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16
SES SES SES SES SES SES SES SES SES SES SES SES SES SES SES SES
Panellus stipticus (Bull.) P. Karst. Tricholoma terreum (Schaeff.) Quel. Tricholoma virgatum (Fr.) P. Kumm. Entoloma sinuatum (Bull.) P. Kumm. Boletus edulis Bull. Boletus luridus Schaeff. Suillus granulatus (L.) Snell. Amanita muscaria var. muscaria (L.) Hook. Amanita pantherina (DC.) Krombh. Agaricus arvensis Schaeff. Agaricus porphyrizon P.D. Onon Agaricus silvicola (Vittad.) Peck Leucoagaricus leucothites (Vittad.) M. Moser Leucoagaricus nympharum (Kalchbr.) Bon Macrolepiota procera (Scop. ex Fr.) Sing. Russula foetens (Pers.) Fr.
On stumps In woods In woods On soil In woodland In broad-leaved woods Under Pinus pinea Under birch tree In woodland Amongst grass in pasture On sandy soils In woods In gardens In gardens In forests Under trees
Inedible Edible Inedible Poisonous Excellent Edible Edible Poisonous Poisonous Excellent Edible Good Poisonous Edible Excellent Inedible
Tricholomataceae Tricholomataceae Tricholomataceae Entolomataceae Boletaceae Boletaceae Suillaceae Pluteaceae Pluteaceae Agaricaceae Agaricaceae Agaricaceae Agaricaceae Agaricaceae Agaricaceae Russulaceae
2168 2323 2332 2297 2193 2162 2254 2123 2007 2222 2249 2335 2286 2229 2161 2049
808
M. Tuzen et al. / Food Control 18 (2007) 806–810
Table 3 The levels of selenium, cadmium, iron, copper, manganese and zinc in mushroom species (lg/g dry matter), N = 3 Mushroom species
Se
Cd
Fe
Cu
Mn
Zn
Panellus stipticus Tricholoma terreum Tricholoma virgatum Entoloma sinuatum Boletus edulis Boletus luridus Suillus granulatus Amanita muscaria Amanita pantherina Agaricus arvensis Agaricus porphyrizon Agaricus silvicola Leucoagaricus leucothites Leucoagaricus nympharum Macrolepiota procera Russula foetens
0.54 ± 0.04 1.32 ± 0.10 4.50 ± 0.32 6.80 ± 0.53 9.89 ± 0.88 1.96 ± 0.15 2.63 ± 0.20 0.85 ± 0.09 10.8 ± 10.9 2.54 ± 0.17 5.32 ± 0.46 1.23 ± 0.10 0.93 ± 0.10 3.28 ± 0.26 6.69 ± 0.52 2.79 ± 0.20
1.8 ± 0.1 2.3 ± 0.2 1.2 ± 0.1 2.1 ± 0.2 1.1 ± 0.1 1.9 ± 0.1 1.5 ± 0.2 2.4 ± 0.2 1.6 ± 0.1 2.5 ± 0.3 1.8 ± 0.1 2.4 ± 0.2 1.4 ± 0.1 0.9 ± 0.1 2.3 ± 0.2 1.4 ± 0.1
680 ± 55 963 ± 74 238 ± 25 530 ± 44 764 ± 65 324 ± 30 658 ± 55 187 ± 17 985 ± 69 740 ± 60 549 ± 46 258 ± 23 590 ± 55 432 ± 27 387 ± 32 753 ± 66
43.3 ± 3.6 32.8 ± 2.5 21.4 ± 2.1 64.8 ± 5.9 20.1 ± 2.2 18.9 ± 1.7 35.8 ± 3.3 33.6 ± 2.5 19.7 ± 1.8 44.8 ± 3.9 19.3 ± 1.5 36.8 ± 3.2 42.4 ± 2.1 27.5 ± 2.2 36.8 ± 3.3 27.7 ± 2.5
89.5 ± 7.3 120 ± 10 75.2 ± 6.3 88.4 ± 6.9 96.3 ± 7.4 123 ± 15 77.5 ± 6.2 66.3 ± 5.1 53.5 ± 3.4 87.5 ± 7.6 88.9 ± 5.4 68.5 ± 5.1 130 ± 12 66.3 ± 2.6 101 ± 10 67.2 ± 5.3
156 ± 14 88.3 ± 6.8 126 ± 11 198 ± 16 158 ± 14 56.7 ± 4.8 59.8 ± 4.3 86.6 ± 7.1 73.5 ± 6.5 85.2 ± 6.1 58.6 ± 4.6 85.3 ± 5.2 59.3 ± 4.1 96.4 ± 6.3 64.1 ± 5.8 44.7 ± 3.2
44.7–198 lg/g for zinc, 187–985 lg/g for iron, 0.54– 10.8 lg/g for selenium and 0.9–2.5 lg/g for cadmium. The trace metal content in the mushrooms are mainly affected by acidic and organic matter content of their ecosystem and soil (Gast, Jansen, Bierling, & Haanstra, 1988). The uptake of metal ions in mushrooms is in many respects different from plants. For this reason the concentration variations of metals depend on mushroom species and their ecosystems (Seeger, 1982). The lower and higher selenium concentrations were 0.54 lg/g in Panellus stipticus and 10.8 lg/g in Amanita pantherina, respectively. Selenium contents of mushroom samples in the literature have been reported in the range of 0.05–37 lg/g (Piepponen, Liukkonen-Lilja, & Kuusi, 1983), 1.30–21.5 lg/g (Huerta, Sanchez, & Sanz-Medel, 2005), 1–367 lg/g (Kalacˇ & Svoboda, 2000), 0.17–975 lg/ kg (Agrahar-Murugkar & Subbulakshmi, 2005). Our selenium values are in agreement with reported in the literature. Knowledge on roles of trace elements in physiology of mushroom has been limited. Concentrations of the elements in fruiting bodies are generally species-dependent. Substrate composition is an important factor, but great differences exist in uptake of individual metals (Gast et al., 1988; Kalacˇ & Svoboda, 2000). Selenium occurrence in fruiting bodies has been assessed, preferably from the nutritional point of view as a potential source of this deficient element. High selenium content was found in Boletus edulis as 9.89 lg/g in this study. Bioavailability of selenium from Boletus edulis was found to be fairly low (Mutanen, 1986). Beside the total content of selenium, the chemical form in which selenium is present is also most important due to the differences in bioavailability and toxicity of the different forms (Mazej, Falnoga, Veber, & Stibilj, 2006). It has also been reported that soluble selenium species present in selenised mushrooms corresponded mostly to low molecular weight compounds (<10 kDa). Selenocystine, Se(IV), selenomethionine and Se-methylselenocysteine species have been already identified in Se-enriched mushrooms
together with a number of unknown selenocompounds. Nowadays selenium is recognized as an essential micronutrient in animal and humans, playing important biological roles as antioxidant, as a regulator of thyroid hormone metabolism or as anti-carcinogenic agent. Some mushrooms, when grown in soils with high selenium contents, are able to accumulate selenium. Boletus edulis, Lycoperdon perlatum, Agaricus, Albatrellus pes-caprae are known high selenium accumulating mushroom species (Huerta et al., 2005). According to Stijve and Besson (1976), the mechanism by which some heavy metals are accumulated is somewhat obscure although it seems to be associated with a chelation reaction with the sulphydryl groups of protein and especially with methionine. Cadmium is known as a principal toxic element, since it inhibits many life processes (Vetter, 1987, 1993). Mushroom, in particular, can be very rich in cadmium. Cadmium accumulation has been demonstrated in literature (Schmitt & Meisch, 1985). The highest and the lowest cadmium concentration found were 2.5 lg/g in Agaricus arvensis and 0.9 lg/g in Leucoagaricus nympharum, respectively. Cadmium contents of mushroom samples in the literature have been reported in the range of 0.81–7.50 lg/g (Svoboda, Zimmermannova, & Kalacˇ, 2000), 0.14–0.95 lg/g (Soylak, Saracoglu, Tuzen, & Mendil, 2005), 0.28–1.6 lg/g (Mendil, Uluozlu, Tuzen, Hasdemir, & Sari, 2005), 0.12– 2.60 lg/g (Malinowska, Szefer, & Falandaysz, 2004). Our cadmium values are in agreement with reported in the literature. The information on chemical forms of cadmium in mushrooms has been very limited. From Agaricus macrosporus cadmium–mycophosphatin was isolated, phosphoglycoprotein of molecular weight 12 000 Da lacking sulphur, with a high proportion of acidic amino acids, glucose and galactose. Moreover, four low-molecular glycoproteins containing sulphur and binding cadmium were isolated (Meisch & Schmitt, 1986). No metallothioneines were found in fruiting bodies of cultivated Agaricus bisporus (Esser & Brunnert, 1986). Cadmium is accumulated mainly
M. Tuzen et al. / Food Control 18 (2007) 806–810
in kidneys, spleen and liver and its level in blood serum increases considerably following mushroom consumption (Kalacˇ & Svoboda, 2000). The fact that toxic metals are present in high concentrations in mushrooms is of particular importance in relation to the FAO/WHO (1976) standards for Pb and Cd as toxic metals. The maximum permissible doses for an adult are 3 mg Pb and 0.5 mg Cd per week, but the recommended doses are only one-fifth of those quantities. The iron content of the mushrooms ranged from 187 lg/g in Suillus granulatus to 985 lg/g in Amanita pantherina. Iron values in mushroom samples have been reported in the range of 31.3–1190 lg/g (Sesli & Tuzen, 1999), 568–3904 lg/g (Turkekul, Elmastas, & Tuzen, 2004), 56.1–7162 lg/g (Isiloglu, Yilmaz, & Merdivan, 2001), 102–1580 lg/g (Soylak et al., 2005), 30–150 lg/g (Kalacˇ & Svoboda, 2000), respectively. Our iron values are in agreement with reported in the literature. It is known that adequate iron in a diet is very important for decreasing the incidence of anemia. The copper levels range from 18.9 to 64.8 lg/g for Boletus luridus and Entoloma sinuatum, respectively in this study. Copper contents of mushroom samples in the literature have been reported in the range of 4.71–51.0 lg/g (Tuzen, Ozdemir, & Demirbas, 1998), 10.3–145 lg/g (Sesli & Tuzen, 1999), 34.5–83.0 lg/g (Isiloglu et al., 2001), 10.0– 14.0 lg/g (Sivrikaya, Bacak, Sarac¸basi, Toroglu, & Eroglu, 2002), 13.4–50.6 lg/g (Soylak et al., 2005), respectively. Copper contents found in this study are in agreement with reported in the literature. Copper concentrations in the accumulating mushroom species are usually 100–300 mg/ kg dry matter, which is not considered a health risk (Kalacˇ & Svoboda, 2000). Copper contents in mushrooms higher than those in vegetables should be considered as a nutritional source of the element. Nevertheless, for people, bioavailability from mushrooms was reported to be low, due to limited absorption from the small intestine (Schellman, Hilz, & Opitz, 1980). The manganese content of the mushrooms studied in the present work ranged from 53.4 lg/g in Amanita pantherina to 130 lg/g in Leucoagaricus leucothites. The reported manganese values in the literature for mushrooms were 14.2–69.7 lg/g, 21.7–74.3 lg/g, 7.1–81.3 lg/g (Isildak, Turkekul, Elmastas, & Tuzen, 2004; Soylak et al., 2005; Tuzen, 2003), respectively. Our manganese values are in agreement with reported in the literature. Mushrooms are known as zinc accumulator and sporophore: substrate ratio for Zn ranges from 1 to 10 mg/kg (Bano, Nagaraja, Vibhakar, & Kapur, 1981; Isiloglu et al., 2001). The zinc content was the lowest (44.7 lg/g) in Russula foetens, whereas in Entoloma sinuatum, it was the highest (198 lg/g). Zinc concentrations of mushroom samples in the literature have been reported in the range of 33.5–89.5 lg/g (Soylak et al., 2005); 29.3–158 lg/g (Isiloglu et al., 2001), 45–188 lg/g (Tuzen, 2003). The levels of essential elements in mushroom species were found higher than toxic elements. Some mushrooms species are accumulated trace elements at high ratio as
809
Entoloma sinuatum for Cu and Zn, Leucoagaricus leucothites for Mn, Amanita pantherina for Fe and Se, Agaricus arvensis for Cd. Generally, the highest element concentrations were found in poisonous mushrooms species. The results obtained for trace elements in analyzed mushroom species were acceptable to human consumption at nutritional and toxic levels. It has been reported that some mushroom species collected from polluted area should not be consumed at all (Svoboda et al., 2000). Acknowledgements We thank Miss. S. Demirel for his help on in the experiments. The authors are grateful for the financial support of the TUBITAK (Project No: 104 T 448). References Agrahar-Murugkar, D., & Subbulakshmi, G. (2005). Nutritional value of edible wild mushrooms collected from the Khasi hills of Meghalaya. Food Chemistry, 89(4), 599. Bano, Z., Nagaraja, K., Vibhakar, S., & Kapur, O. P. (1981). Mineral and the heavy metal contents in the sporophores of pleurotus species. Mushroom Newsletter Tropics, 2, 3–7. Breitenbach, J., & Kra¨nzlin, F. (2000). Fungi of Switzerland (Vol. 2, 3, 4, 5). Lucerne: Verlag Mykologia. Esser, J., & Brunnert, H. (1986). Isolation and partial purification of cadmium-binding components from fruiting bodies of Agaricus bisporus. Environmental Pollution A, 41, 263–275. FAO/WHO, (1976). List of maximum levels recommended for contaminants by the Joint FAO/WHO Codex Alimentarius Commission. (Vol. 3, pp. 1–8). Second Series. CAC/FAL, Rome. Gast, C. H., Jansen, E., Bierling, J., & Haanstra, L. (1988). Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere, 17, 789–799. Huerta, V. D., Sanchez, M. L. F., & Sanz-Medel, A. (2005). Qualitative and quantitative speciation analysis of water soluble selenium in three edible wild mushroom species by liquid chromatography using postcolumn isotope dilution ICP-MS. Analytica Chimica Acta, 538(1–2), 99–105. Isildak, O., 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 Chemistry, 86, 547–552. Isiloglu, M., Yilmaz, F., & Merdivan, M. (2001). Concentrations of trace elements in wild edible mushrooms. Food Chemistry, 73, 163–175. Kalacˇ, P., & Svoboda, L. (2000). A review of trace element concentrations in edible mushrooms. Food Chemistry, 69, 273–281. Malinowska, E., Szefer, P., & Falandaysz, J. (2004). Metals bioaccumulation by bay bolete, Xerocomus badius, from selected sites in Poland. Food Chemistry, 84(3), 405–416. Manzi, P., Aguzzi, A., & Pizzoferrato, L. (2001). Nutritional value of mushrooms widely consumed in Italy. Food Chemistry, 73, 321–325. Mazej, D., Falnoga, I., Veber, M., & Stibilj, V. (2006). Determination of selenium species in plant leaves by HPLC–UV–HG–AFS. Talanta, 68, 558–568. Meisch, H.-U., & Schmitt, J. A. (1986). Characterization studies on cadmium–mycophosphatin from the mushroom Agaricus macrosporus. Environmental Health Perspectives, 65, 29–32. Mendil, D., Uluozlu, O. D., Tuzen, M., Hasdemir, E., & Sari, H. (2005). Trace metal levels in mushroom samples from Ordu, Turkey. Food Chemistry, 91, 463–467. Mutanen, M. (1986). Bioavailability of selenium in mushrooms, Boletus edulis, to young women. International Journal for Vitamin and Nutrition Research, 65, 297–301.
810
M. Tuzen et al. / Food Control 18 (2007) 806–810
Onianwa, P. C., Adeyemo, A. O., Idowu, O. E., & Ogabiela, E. E. (2001). Copper and zinc contents of Nigerian foods and estimates of the adult dietary intakes. Food Chemistry, 72, 89–95. Orak, H., Altun, M., & Ercag, E. (2005). Survey of heavy metals in Turkish white cheese. Italian Journal of Food Science, 17, 95–100. Piepponen, S., Liukkonen-Lilja, H., & Kuusi, T. (1983). The selenium content of edible mushroom in Finland. Zeitschrift fur Lebensmittel– Untersuchung und -Forschung, 177, 257–260. Radwan, M. A., & Salama, A. K. (in press). Market basket survey for some heavy metals in Egyptian fruits and vegetables. Food and Chemical Toxicology. Schellman, B., Hilz, M. J., & Opitz, O. (1980). Cadmium an kopfer ausscheidung nach aufnahme von champignon-mahlzeiten. Zeitschrift fur Lebensmittel-Untersuchung und -Forschung, 171, 189–192. Schmitt, J. A., & Meisch, H. U. (1985). Cadmium in mushrooms, distribution growth effects and binding. Trace Elements in Medicine, 2, 163–166. Seeger, R. (1982). Toxische schwermetalle in Pilzen. Deutsche Apotheke Zeitschrift, 122, 1835–1844. Sesli, E., & Tuzen, M. (1999). Levels of trace elements in the fruiting bodies of macrofungi growing in the East Black Sea region of Turkey. Food Chemistry, 65, 453–460. Sivrikaya, H., Bacak, L., Sarac¸basi, A., Toroglu, I., & Eroglu, H. (2002). Trace elements in pleurotus sajor-caju cultivated on chemithermomechanical pulp for bio-bleaching. Food Chemistry, 79, 173–176. Soylak, M., Colak, H., Tuzen, M., Turkoglu, O., & Elci, L. (2006). Comparison of digestion procedures for commercial powdered soup samples for the determination of their trace heavy metal contents by AAS. Journal of Food and Drug Analysis, 14, 62–67.
Soylak, M., Karatepe, A. U., Elci, L., & Dogan, M. (2003). Column preconcentration/separation and atomic absorption spectrometric determinations of some heavy metals in table salt samples using amberlite XAD-1180. Turkish Journal of Chemistry, 27, 235– 242. Soylak, M., Saracoglu, S., Tuzen, M., & Mendil, D. (2005). Determination of trace metals in mushroom samples from Kayseri, Turkey. Food Chemistry, 92, 649–652. Stijve, T., & Besson, R. (1976). Mercury, cadmium and selenium content of mushroom species belonging to the Agaricus. Chemosphere, 2, 151–158. Svoboda, L., Zimmermannova, K., & Kalacˇ, P. (2000). Concentrations of mercury, cadmium, lead, and copper in fruiting bodies of edible mushrooms in an emission area of a copper smelter and a mercury smelter. The Science of the Total Environment, 246, 61–67. Turkekul, I., Elmastas, M., & Tuzen, M. (2004). Determination of iron, copper, manganese, zinc, lead, and cadmium in mushroom samples from Tokat, Turkey. Food Chemistry, 84, 389–392. Tuzen, M. (2003). Determination of heavy metals in soil, mushroom and plant samples by atomic absorption spectrometry. Microchemical Journal, 74, 289–297. Tuzen, M., Ozdemir, M., & Demirbas, A. (1998). Study of heavy metals in some cultivated and uncultivated mushrooms of Turkish origin. Food Chemistry, 63(2), 247–251. Vetter, J. (1987). Mineral elements in higher fungi. Clusiana (Mikologiai Ko¨zlemenyek), 26, 125–150. Vetter, J. (1993). Toxic elements in certain higher fungi. Food Chemistry, 48, 207–208.
Trace element levels of mushroom species from East Black Sea region of Turkey Mustafa Tuzen a, Ertugrul Sesli b, Mustafa Soylak b
c,*
a Gaziosmanpasa University, Faculty of Science and Arts, Department of Chemistry, 60250 Tokat, Turkey Karadeniz Technical University, Faculty of Fatih Education, Department of Biological Education, 61335 So¨gutlu, Trabzon, Turkey c Erciyes University, Faculty of Art and Science, Department of Chemistry, 38039 Kayseri, Turkey
Received 17 November 2005; received in revised form 5 April 2006; accepted 10 April 2006
Abstract The levels of trace metals of mushroom samples collected from East Black Sea region of Turkey were determined by flame and graphite furnace atomic absorption spectrometry after microwave digestion method. The accuracy of the method was corrected by standard reference material (NIST SRM 1573a Tomato Leaves). The contents of investigated trace metals in mushroom samples were found to be in the range of 18.9–64.8 lg/g for copper, 53.5–130 lg/g for manganese, 44.7–198 lg/g for zinc, 187–985 lg/g for iron, 0.54–10.8 lg/g for selenium and 0.9–2.5 lg/g for cadmium. Mushrooms species in the highest levels of trace elements were found Entoloma sinuatum for Cu and Zn, Leucoagaricus leucothites for Mn, Amanita pantherina for Fe and Se, Agaricus arvensis for Cd. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Trace elements; Mushroom; Atomic absorption spectrometry; East Black Sea region – Turkey
1. Introduction The consumption of wild edible mushrooms is increasing, even in the developed world, due to a good content of proteins as well as a higher content of trace minerals (Agrahar-Murugkar & Subbulakshmi, 2005). Wild mushrooms are a popular food source in Turkey. Mushrooms have along history of use in traditional Chinese medicine. Mushrooms have also been reported as therapeutic foods, useful in preventing diseases such as hypertension, hypercholesterolemia, and cancer. These functional characteristics are mainly due to their chemical composition (Manzi, Aguzzi, & Pizzoferrato, 2001). Due to positive and negative effects and the toxicity of heavy metals on both human health and the environment, many researchers are interested in the analysis of trace metal contents of environmental samples and *
Corresponding author. Tel./fax: +90 352 4374933. E-mail addresses: [email protected] (M. Tuzen), soylak@erciyes. edu.tr (M. Soylak). 0956-7135/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2006.04.003
especially foods (Orak, Altun, & Ercag, 2005; Radwan & Salama, 2006; Soylak, Colak, Tuzen, Turkoglu, & Elci, 2006). Accurate and adequate food composition data are invaluable for estimating the adequacy of intakes of essential nutrients and assessing exposure risks from intake of toxic non-essential heavy metals (Onianwa, Adeyemo, Idowu, & Ogabiela, 2001; Soylak, Karatepe, Elci, & Dogan, 2003). Turkey can be separated into seven geographic regions. One of them is the Black Sea region. The Black Sea region can be separated into three smaller geographic regions. The East Black Sea region is one of them. In this region, the climate is mild and rainy. The seasons are normally wet with mild temperatures. The climate during the year, especially, in spring and autumn, is ideal for mushroom growth (Sesli & Tuzen, 1999). In the present study, the contents of selenium, cadmium, iron, copper, manganese and zinc in mushroom samples collected from East Black Sea region of Turkey were determined by flame and/or graphite furnace atomic absorption spectrometry after microwave digestion.
M. Tuzen et al. / Food Control 18 (2007) 806–810
2. Materials and methods Forty eight samples including 16 different mushroom species were collected during field trips in different localities of East Black Sea region of Turkey in 2004. Main ecological and morphological properties of mushroom were noted at the field. The specimens were examined in the laboratory at an earliest convenient time after collection. All the spore measurements were calculated from at least 20 individual measurements using research microscopes. Excised pieces of mushroom were moistened by addition of a few drops of Clemencon’s solution [20 ml concentrated ammonia + 1 g glycerine + 80 ml 96% ethanol] and then sectioned. The fungi (Table 1) were identified according to Breitenbach and Kra¨nzlin (1986, 1991, 1995, 2000). Some specimens were deposited at the personal fungarium of Faculty of Fatih Education at Karadeniz Technical University in Trabzon Province of Turkey. The samples were dried at 105 °C for 24 h for chemical investigations. Dried samples were homogenized using an agate homogenizer and stored in polyethylene bottles until analysis. All the plastic and glassware were cleaned by soaking with the contact overnight in a 10% nitric acid solution and then rinsed with deionized water. One gram of sample was digested with 6 ml of concentrated HNO3 (Suprapure, Merck) and 2 ml of concentrated H2O2 (Suprapure, Merck) in Milestone Ethos D model microwave digestion system (maximum pressure 1450 psi and maximum temperature 300 °C) and diluted to 10 ml with double deionized water (Milli-Q Millipore 18.2 MX cm 1 resistivity). A blank digest was carried out in the same way (digestion conditions for microwave system were applied as 2 min for 250 W, 2 min for 0 W, 6 min for 250 W, 5 min for 400 W, 8 min for 550 W, vent: 8 min, respectively). The accuracy of the method was verified by standard reference materials (NIST SRM 1573a Tomato Leaves). A Perkin–Elmer Analyst 700 model atomic absorption spectrometer with deuterium background cor-
807
rector was used in this study. Selenium and cadmium levels in the mushroom samples were determined by HGA graphite furnace using argon as inert gas. The other elements were determined in air–acetylene flame. 3. Results and discussion Detection limit is defined as the concentration corresponding to three times the standard deviation of ten blanks. Detection limit values of elements as milligram per liter in flame AAS were found to be 0.005 for Cu, 0.010 for Zn, 0.008 for Fe, 0.009 for Mn. Selenium and cadmium were below detection limit of flame AAS. Se and Cd were determined using graphite furnace AAS. The recovery values were nearly quantitative for microwave digestion method. The relative standard deviations were less than 10% for all investigated elements. T-test was used in this study (p < 0.05). The accuracy of the method was evaluated by means of trace metals determination in standard reference material (SRM). The achieved results were in good agreement with certified values. The results for this study are given in Table 2. Trace metal levels in the analysed samples are listed in Table 3. All metal concentrations were determined on a dry weight basis. The concentrations of investigated trace metals in mushroom samples were found to be in the range of 18.9–64.8 lg/g for copper, 53.5–130 lg/g for manganese, Table 2 Observed and certified values of trace metals in NIST SRM 1573a Tomato Leaves, N = 4 Element
Certified value (lg/g)
Our value (lg/g)
Recovery (%)
Cu Zn Mn Fe Se Cd
4.7 30.9 246 368 0.054 1.52
4.64 ± 0.25 29.5 ± 1.9 238.9 ± 13.3 361.5 ± 25.3 0.052 ± 0.004 1.53 ± 0.10
99 95 97 98 96 101
Table 1 Habitat, edibility and names of mushrooms No
Fungarium
Name of mushroom
Habitat
Edibility
Family
01 02 03 04 05 06 07 08 09 10 11 12 13 14 15 16
SES SES SES SES SES SES SES SES SES SES SES SES SES SES SES SES
Panellus stipticus (Bull.) P. Karst. Tricholoma terreum (Schaeff.) Quel. Tricholoma virgatum (Fr.) P. Kumm. Entoloma sinuatum (Bull.) P. Kumm. Boletus edulis Bull. Boletus luridus Schaeff. Suillus granulatus (L.) Snell. Amanita muscaria var. muscaria (L.) Hook. Amanita pantherina (DC.) Krombh. Agaricus arvensis Schaeff. Agaricus porphyrizon P.D. Onon Agaricus silvicola (Vittad.) Peck Leucoagaricus leucothites (Vittad.) M. Moser Leucoagaricus nympharum (Kalchbr.) Bon Macrolepiota procera (Scop. ex Fr.) Sing. Russula foetens (Pers.) Fr.
On stumps In woods In woods On soil In woodland In broad-leaved woods Under Pinus pinea Under birch tree In woodland Amongst grass in pasture On sandy soils In woods In gardens In gardens In forests Under trees
Inedible Edible Inedible Poisonous Excellent Edible Edible Poisonous Poisonous Excellent Edible Good Poisonous Edible Excellent Inedible
Tricholomataceae Tricholomataceae Tricholomataceae Entolomataceae Boletaceae Boletaceae Suillaceae Pluteaceae Pluteaceae Agaricaceae Agaricaceae Agaricaceae Agaricaceae Agaricaceae Agaricaceae Russulaceae
2168 2323 2332 2297 2193 2162 2254 2123 2007 2222 2249 2335 2286 2229 2161 2049
808
M. Tuzen et al. / Food Control 18 (2007) 806–810
Table 3 The levels of selenium, cadmium, iron, copper, manganese and zinc in mushroom species (lg/g dry matter), N = 3 Mushroom species
Se
Cd
Fe
Cu
Mn
Zn
Panellus stipticus Tricholoma terreum Tricholoma virgatum Entoloma sinuatum Boletus edulis Boletus luridus Suillus granulatus Amanita muscaria Amanita pantherina Agaricus arvensis Agaricus porphyrizon Agaricus silvicola Leucoagaricus leucothites Leucoagaricus nympharum Macrolepiota procera Russula foetens
0.54 ± 0.04 1.32 ± 0.10 4.50 ± 0.32 6.80 ± 0.53 9.89 ± 0.88 1.96 ± 0.15 2.63 ± 0.20 0.85 ± 0.09 10.8 ± 10.9 2.54 ± 0.17 5.32 ± 0.46 1.23 ± 0.10 0.93 ± 0.10 3.28 ± 0.26 6.69 ± 0.52 2.79 ± 0.20
1.8 ± 0.1 2.3 ± 0.2 1.2 ± 0.1 2.1 ± 0.2 1.1 ± 0.1 1.9 ± 0.1 1.5 ± 0.2 2.4 ± 0.2 1.6 ± 0.1 2.5 ± 0.3 1.8 ± 0.1 2.4 ± 0.2 1.4 ± 0.1 0.9 ± 0.1 2.3 ± 0.2 1.4 ± 0.1
680 ± 55 963 ± 74 238 ± 25 530 ± 44 764 ± 65 324 ± 30 658 ± 55 187 ± 17 985 ± 69 740 ± 60 549 ± 46 258 ± 23 590 ± 55 432 ± 27 387 ± 32 753 ± 66
43.3 ± 3.6 32.8 ± 2.5 21.4 ± 2.1 64.8 ± 5.9 20.1 ± 2.2 18.9 ± 1.7 35.8 ± 3.3 33.6 ± 2.5 19.7 ± 1.8 44.8 ± 3.9 19.3 ± 1.5 36.8 ± 3.2 42.4 ± 2.1 27.5 ± 2.2 36.8 ± 3.3 27.7 ± 2.5
89.5 ± 7.3 120 ± 10 75.2 ± 6.3 88.4 ± 6.9 96.3 ± 7.4 123 ± 15 77.5 ± 6.2 66.3 ± 5.1 53.5 ± 3.4 87.5 ± 7.6 88.9 ± 5.4 68.5 ± 5.1 130 ± 12 66.3 ± 2.6 101 ± 10 67.2 ± 5.3
156 ± 14 88.3 ± 6.8 126 ± 11 198 ± 16 158 ± 14 56.7 ± 4.8 59.8 ± 4.3 86.6 ± 7.1 73.5 ± 6.5 85.2 ± 6.1 58.6 ± 4.6 85.3 ± 5.2 59.3 ± 4.1 96.4 ± 6.3 64.1 ± 5.8 44.7 ± 3.2
44.7–198 lg/g for zinc, 187–985 lg/g for iron, 0.54– 10.8 lg/g for selenium and 0.9–2.5 lg/g for cadmium. The trace metal content in the mushrooms are mainly affected by acidic and organic matter content of their ecosystem and soil (Gast, Jansen, Bierling, & Haanstra, 1988). The uptake of metal ions in mushrooms is in many respects different from plants. For this reason the concentration variations of metals depend on mushroom species and their ecosystems (Seeger, 1982). The lower and higher selenium concentrations were 0.54 lg/g in Panellus stipticus and 10.8 lg/g in Amanita pantherina, respectively. Selenium contents of mushroom samples in the literature have been reported in the range of 0.05–37 lg/g (Piepponen, Liukkonen-Lilja, & Kuusi, 1983), 1.30–21.5 lg/g (Huerta, Sanchez, & Sanz-Medel, 2005), 1–367 lg/g (Kalacˇ & Svoboda, 2000), 0.17–975 lg/ kg (Agrahar-Murugkar & Subbulakshmi, 2005). Our selenium values are in agreement with reported in the literature. Knowledge on roles of trace elements in physiology of mushroom has been limited. Concentrations of the elements in fruiting bodies are generally species-dependent. Substrate composition is an important factor, but great differences exist in uptake of individual metals (Gast et al., 1988; Kalacˇ & Svoboda, 2000). Selenium occurrence in fruiting bodies has been assessed, preferably from the nutritional point of view as a potential source of this deficient element. High selenium content was found in Boletus edulis as 9.89 lg/g in this study. Bioavailability of selenium from Boletus edulis was found to be fairly low (Mutanen, 1986). Beside the total content of selenium, the chemical form in which selenium is present is also most important due to the differences in bioavailability and toxicity of the different forms (Mazej, Falnoga, Veber, & Stibilj, 2006). It has also been reported that soluble selenium species present in selenised mushrooms corresponded mostly to low molecular weight compounds (<10 kDa). Selenocystine, Se(IV), selenomethionine and Se-methylselenocysteine species have been already identified in Se-enriched mushrooms
together with a number of unknown selenocompounds. Nowadays selenium is recognized as an essential micronutrient in animal and humans, playing important biological roles as antioxidant, as a regulator of thyroid hormone metabolism or as anti-carcinogenic agent. Some mushrooms, when grown in soils with high selenium contents, are able to accumulate selenium. Boletus edulis, Lycoperdon perlatum, Agaricus, Albatrellus pes-caprae are known high selenium accumulating mushroom species (Huerta et al., 2005). According to Stijve and Besson (1976), the mechanism by which some heavy metals are accumulated is somewhat obscure although it seems to be associated with a chelation reaction with the sulphydryl groups of protein and especially with methionine. Cadmium is known as a principal toxic element, since it inhibits many life processes (Vetter, 1987, 1993). Mushroom, in particular, can be very rich in cadmium. Cadmium accumulation has been demonstrated in literature (Schmitt & Meisch, 1985). The highest and the lowest cadmium concentration found were 2.5 lg/g in Agaricus arvensis and 0.9 lg/g in Leucoagaricus nympharum, respectively. Cadmium contents of mushroom samples in the literature have been reported in the range of 0.81–7.50 lg/g (Svoboda, Zimmermannova, & Kalacˇ, 2000), 0.14–0.95 lg/g (Soylak, Saracoglu, Tuzen, & Mendil, 2005), 0.28–1.6 lg/g (Mendil, Uluozlu, Tuzen, Hasdemir, & Sari, 2005), 0.12– 2.60 lg/g (Malinowska, Szefer, & Falandaysz, 2004). Our cadmium values are in agreement with reported in the literature. The information on chemical forms of cadmium in mushrooms has been very limited. From Agaricus macrosporus cadmium–mycophosphatin was isolated, phosphoglycoprotein of molecular weight 12 000 Da lacking sulphur, with a high proportion of acidic amino acids, glucose and galactose. Moreover, four low-molecular glycoproteins containing sulphur and binding cadmium were isolated (Meisch & Schmitt, 1986). No metallothioneines were found in fruiting bodies of cultivated Agaricus bisporus (Esser & Brunnert, 1986). Cadmium is accumulated mainly
M. Tuzen et al. / Food Control 18 (2007) 806–810
in kidneys, spleen and liver and its level in blood serum increases considerably following mushroom consumption (Kalacˇ & Svoboda, 2000). The fact that toxic metals are present in high concentrations in mushrooms is of particular importance in relation to the FAO/WHO (1976) standards for Pb and Cd as toxic metals. The maximum permissible doses for an adult are 3 mg Pb and 0.5 mg Cd per week, but the recommended doses are only one-fifth of those quantities. The iron content of the mushrooms ranged from 187 lg/g in Suillus granulatus to 985 lg/g in Amanita pantherina. Iron values in mushroom samples have been reported in the range of 31.3–1190 lg/g (Sesli & Tuzen, 1999), 568–3904 lg/g (Turkekul, Elmastas, & Tuzen, 2004), 56.1–7162 lg/g (Isiloglu, Yilmaz, & Merdivan, 2001), 102–1580 lg/g (Soylak et al., 2005), 30–150 lg/g (Kalacˇ & Svoboda, 2000), respectively. Our iron values are in agreement with reported in the literature. It is known that adequate iron in a diet is very important for decreasing the incidence of anemia. The copper levels range from 18.9 to 64.8 lg/g for Boletus luridus and Entoloma sinuatum, respectively in this study. Copper contents of mushroom samples in the literature have been reported in the range of 4.71–51.0 lg/g (Tuzen, Ozdemir, & Demirbas, 1998), 10.3–145 lg/g (Sesli & Tuzen, 1999), 34.5–83.0 lg/g (Isiloglu et al., 2001), 10.0– 14.0 lg/g (Sivrikaya, Bacak, Sarac¸basi, Toroglu, & Eroglu, 2002), 13.4–50.6 lg/g (Soylak et al., 2005), respectively. Copper contents found in this study are in agreement with reported in the literature. Copper concentrations in the accumulating mushroom species are usually 100–300 mg/ kg dry matter, which is not considered a health risk (Kalacˇ & Svoboda, 2000). Copper contents in mushrooms higher than those in vegetables should be considered as a nutritional source of the element. Nevertheless, for people, bioavailability from mushrooms was reported to be low, due to limited absorption from the small intestine (Schellman, Hilz, & Opitz, 1980). The manganese content of the mushrooms studied in the present work ranged from 53.4 lg/g in Amanita pantherina to 130 lg/g in Leucoagaricus leucothites. The reported manganese values in the literature for mushrooms were 14.2–69.7 lg/g, 21.7–74.3 lg/g, 7.1–81.3 lg/g (Isildak, Turkekul, Elmastas, & Tuzen, 2004; Soylak et al., 2005; Tuzen, 2003), respectively. Our manganese values are in agreement with reported in the literature. Mushrooms are known as zinc accumulator and sporophore: substrate ratio for Zn ranges from 1 to 10 mg/kg (Bano, Nagaraja, Vibhakar, & Kapur, 1981; Isiloglu et al., 2001). The zinc content was the lowest (44.7 lg/g) in Russula foetens, whereas in Entoloma sinuatum, it was the highest (198 lg/g). Zinc concentrations of mushroom samples in the literature have been reported in the range of 33.5–89.5 lg/g (Soylak et al., 2005); 29.3–158 lg/g (Isiloglu et al., 2001), 45–188 lg/g (Tuzen, 2003). The levels of essential elements in mushroom species were found higher than toxic elements. Some mushrooms species are accumulated trace elements at high ratio as
809
Entoloma sinuatum for Cu and Zn, Leucoagaricus leucothites for Mn, Amanita pantherina for Fe and Se, Agaricus arvensis for Cd. Generally, the highest element concentrations were found in poisonous mushrooms species. The results obtained for trace elements in analyzed mushroom species were acceptable to human consumption at nutritional and toxic levels. It has been reported that some mushroom species collected from polluted area should not be consumed at all (Svoboda et al., 2000). Acknowledgements We thank Miss. S. Demirel for his help on in the experiments. The authors are grateful for the financial support of the TUBITAK (Project No: 104 T 448). References Agrahar-Murugkar, D., & Subbulakshmi, G. (2005). Nutritional value of edible wild mushrooms collected from the Khasi hills of Meghalaya. Food Chemistry, 89(4), 599. Bano, Z., Nagaraja, K., Vibhakar, S., & Kapur, O. P. (1981). Mineral and the heavy metal contents in the sporophores of pleurotus species. Mushroom Newsletter Tropics, 2, 3–7. Breitenbach, J., & Kra¨nzlin, F. (2000). Fungi of Switzerland (Vol. 2, 3, 4, 5). Lucerne: Verlag Mykologia. Esser, J., & Brunnert, H. (1986). Isolation and partial purification of cadmium-binding components from fruiting bodies of Agaricus bisporus. Environmental Pollution A, 41, 263–275. FAO/WHO, (1976). List of maximum levels recommended for contaminants by the Joint FAO/WHO Codex Alimentarius Commission. (Vol. 3, pp. 1–8). Second Series. CAC/FAL, Rome. Gast, C. H., Jansen, E., Bierling, J., & Haanstra, L. (1988). Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere, 17, 789–799. Huerta, V. D., Sanchez, M. L. F., & Sanz-Medel, A. (2005). Qualitative and quantitative speciation analysis of water soluble selenium in three edible wild mushroom species by liquid chromatography using postcolumn isotope dilution ICP-MS. Analytica Chimica Acta, 538(1–2), 99–105. Isildak, O., 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 Chemistry, 86, 547–552. Isiloglu, M., Yilmaz, F., & Merdivan, M. (2001). Concentrations of trace elements in wild edible mushrooms. Food Chemistry, 73, 163–175. Kalacˇ, P., & Svoboda, L. (2000). A review of trace element concentrations in edible mushrooms. Food Chemistry, 69, 273–281. Malinowska, E., Szefer, P., & Falandaysz, J. (2004). Metals bioaccumulation by bay bolete, Xerocomus badius, from selected sites in Poland. Food Chemistry, 84(3), 405–416. Manzi, P., Aguzzi, A., & Pizzoferrato, L. (2001). Nutritional value of mushrooms widely consumed in Italy. Food Chemistry, 73, 321–325. Mazej, D., Falnoga, I., Veber, M., & Stibilj, V. (2006). Determination of selenium species in plant leaves by HPLC–UV–HG–AFS. Talanta, 68, 558–568. Meisch, H.-U., & Schmitt, J. A. (1986). Characterization studies on cadmium–mycophosphatin from the mushroom Agaricus macrosporus. Environmental Health Perspectives, 65, 29–32. Mendil, D., Uluozlu, O. D., Tuzen, M., Hasdemir, E., & Sari, H. (2005). Trace metal levels in mushroom samples from Ordu, Turkey. Food Chemistry, 91, 463–467. Mutanen, M. (1986). Bioavailability of selenium in mushrooms, Boletus edulis, to young women. International Journal for Vitamin and Nutrition Research, 65, 297–301.
810
M. Tuzen et al. / Food Control 18 (2007) 806–810
Onianwa, P. C., Adeyemo, A. O., Idowu, O. E., & Ogabiela, E. E. (2001). Copper and zinc contents of Nigerian foods and estimates of the adult dietary intakes. Food Chemistry, 72, 89–95. Orak, H., Altun, M., & Ercag, E. (2005). Survey of heavy metals in Turkish white cheese. Italian Journal of Food Science, 17, 95–100. Piepponen, S., Liukkonen-Lilja, H., & Kuusi, T. (1983). The selenium content of edible mushroom in Finland. Zeitschrift fur Lebensmittel– Untersuchung und -Forschung, 177, 257–260. Radwan, M. A., & Salama, A. K. (in press). Market basket survey for some heavy metals in Egyptian fruits and vegetables. Food and Chemical Toxicology. Schellman, B., Hilz, M. J., & Opitz, O. (1980). Cadmium an kopfer ausscheidung nach aufnahme von champignon-mahlzeiten. Zeitschrift fur Lebensmittel-Untersuchung und -Forschung, 171, 189–192. Schmitt, J. A., & Meisch, H. U. (1985). Cadmium in mushrooms, distribution growth effects and binding. Trace Elements in Medicine, 2, 163–166. Seeger, R. (1982). Toxische schwermetalle in Pilzen. Deutsche Apotheke Zeitschrift, 122, 1835–1844. Sesli, E., & Tuzen, M. (1999). Levels of trace elements in the fruiting bodies of macrofungi growing in the East Black Sea region of Turkey. Food Chemistry, 65, 453–460. Sivrikaya, H., Bacak, L., Sarac¸basi, A., Toroglu, I., & Eroglu, H. (2002). Trace elements in pleurotus sajor-caju cultivated on chemithermomechanical pulp for bio-bleaching. Food Chemistry, 79, 173–176. Soylak, M., Colak, H., Tuzen, M., Turkoglu, O., & Elci, L. (2006). Comparison of digestion procedures for commercial powdered soup samples for the determination of their trace heavy metal contents by AAS. Journal of Food and Drug Analysis, 14, 62–67.
Soylak, M., Karatepe, A. U., Elci, L., & Dogan, M. (2003). Column preconcentration/separation and atomic absorption spectrometric determinations of some heavy metals in table salt samples using amberlite XAD-1180. Turkish Journal of Chemistry, 27, 235– 242. Soylak, M., Saracoglu, S., Tuzen, M., & Mendil, D. (2005). Determination of trace metals in mushroom samples from Kayseri, Turkey. Food Chemistry, 92, 649–652. Stijve, T., & Besson, R. (1976). Mercury, cadmium and selenium content of mushroom species belonging to the Agaricus. Chemosphere, 2, 151–158. Svoboda, L., Zimmermannova, K., & Kalacˇ, P. (2000). Concentrations of mercury, cadmium, lead, and copper in fruiting bodies of edible mushrooms in an emission area of a copper smelter and a mercury smelter. The Science of the Total Environment, 246, 61–67. Turkekul, I., Elmastas, M., & Tuzen, M. (2004). Determination of iron, copper, manganese, zinc, lead, and cadmium in mushroom samples from Tokat, Turkey. Food Chemistry, 84, 389–392. Tuzen, M. (2003). Determination of heavy metals in soil, mushroom and plant samples by atomic absorption spectrometry. Microchemical Journal, 74, 289–297. Tuzen, M., Ozdemir, M., & Demirbas, A. (1998). Study of heavy metals in some cultivated and uncultivated mushrooms of Turkish origin. Food Chemistry, 63(2), 247–251. Vetter, J. (1987). Mineral elements in higher fungi. Clusiana (Mikologiai Ko¨zlemenyek), 26, 125–150. Vetter, J. (1993). Toxic elements in certain higher fungi. Food Chemistry, 48, 207–208.