The effects of different cooking modes on the 137Cs, 40K, and total K content in Boletus edulis (King Bolete) mushrooms

This study aimed to get an insight into the effects of household processing on the leaching behaviour of 137Cs and 40K from fresh, frozen and dried Boletus edulis (King Bolete) mushrooms. Three processes were investigated—blanching, blanching and pickling, and drying followed by grinding and soaking. The activity concentrations of 137Cs and 40K in the fresh unprocessed mushrooms were 270 Bq kg−1 dry biomass (27 Bq kg−1 whole weight) and 590 Bq kg−1 db (59 Bq kg−1 ww), respectively. Blanching of fresh mushrooms decreased 137Cs activity by 55%, and 40K activity by 34%, and blanching of deep-frozen mushrooms caused a reduction of 52% and 44% (db) (equivalent to whole weight reductions of 37% and 8.5%, and 67% and 22%, respectively). Blanching and pickling of fresh mushrooms decreased 137Cs activity by 83% and 40K activity by 87%, while blanching deep-frozen mushrooms resulted in decreases of 88% and 80% (db) (whole weight decreases of 77% and 81%, and by ~ 84% and 72%, respectively). This study confirms earlier reports that blanching of fresh or frozen mushrooms alone is not as efficient at removing 137Cs as blanching followed by pickling. The study also shows that the initial rate of fruiting body disintegration and pre-preparation (comparing fresh, deep-frozen, or dried and ground) can have an impact on the leaching rate of the water soluble fraction of metallic elements. Electronic supplementary material The online version of this article (10.1007/s11356-020-11147-7) contains supplementary material, which is available to authorized users.


Introduction
Macrofungi exhibit a remarkable aptitude and propensity to bioconcentrate a variety of major and trace mineral constituents, including radioactive elements, in their fruiting bodies (mushrooms) (Falandysz and Borovička 2013). Edible species that grow in the wild were considered as a potentially significant source of human dietary exposure to radiocaesium ( 134/ 137 Cs) from the atmospheric fallout of radioactivity from nuclear weapon testing in the atmosphere and nuclear power plant accidents (Daillant et al. 2013;Kiefer et al. 1965;Rantavaara 2003). In particular, the incident at the Chernobyl nuclear power plant in 1986 led to 137 Cs contamination of wild mushrooms in surrounding European regions (Betti et al. 2017;Daillant et al. 2013;Tucaković et al. 2018). Similarly, the incident at the Fukushima-Daichi nuclear power plant in 2011 caused 137 Cs contamination of locally foraged mushrooms (Cui et al. 2020), without showing any noticeable effect on the wild species collected in continental Asia and Europe (Falandysz et al. 2018;Prand-Stritzko and Steinhauser 2018). Mushrooms preparation techniques, e.g., blanching, boiling, parboiling, pickling, braising, stewing, grilling, frying, soaking (macerating), and also industrial conserving (pickling and canning), have an effect on the content of mineral constituents in processed products (Beresford et al. 2001;Drewnowska et al. 2017;Falandysz et al. 2020a, b;Pankavec et al. 2019;Skibniewska and Smoczyński 1999;Steinhauser and Steinhauser 2016;Stijve 1994). Daillant et al. noted that routine culinary practices using a variety of different treatments were only partly successful in decreasing 137 Cs contents in potential mushroom meals (Daillant et al. 2013). Some practices such as stir-frying and braising cause an increase rather than diminution in 137 Cs and 40 K activity concentrations as well as concentration of mercury (Hg) compounds in the cooked products as the hot oil/processing dehydrates the mushrooms, while substantially preserving the mineral constituents, including 137 Cs (Falandysz et al. , 2020aFalandysz et al. submitted for publication). Culinary processing of mushrooms, depending on the process, may or may not lead to a potential reduction of 137 Cs and other contaminants in mushroom meals and is therefore a potentially important means of modulating human exposure.
This study aimed to study the effects of blanching and blanching followed by pickling on the leaching of 137 Cs and 40 K from processed fresh and frozen fruiting bodies of Boletus edulis. Additionally, dried mushrooms were also ground and soaked in cold water to assess possible leakage of the nuclides. Activity data obtained for the pickled B. edulis were also discussed relative to the activity concentrations of 137 Cs and 40 K in commercially pickled King Bolete and other mushrooms such as Imleria badia (Fr.) Fr. (Bay Bolete) and Suillus luteus (Slippery Jack).

Materials
Eighteen fruiting bodies of Boletus edulis (Bull: Fr.) were collected in the proximity of the village of Osiek in the Tuchola Pinewoods from the north-central region of Poland in 2015 (Fig. 1). The specimens were relatively large sized, well-developed, and in good body condition with white to yellow hymenophores. The mushrooms were carefully cleaned from foreign debris using a plastic knife and brush and separated into caps and stipes. The caps and stipes were cut using a plastic knife into three approximately equivalent pools. The separately pooled caps and stipes were subjected to household treatments including blanching; blanching and pickling; drying, grinding, and macerating; deep-freezing, blanching, and pickling.
In brief, batches of pooled fresh caps and stipes were subjected to blanching and blanching and pickling, and in parallel, a subsamples of pooled caps and stipes in sealed polyethylene bags were deep-frozen (− 20°C) for a week. The frozen subsamples were subjected to blanching and blanching and pickling in the same manner as the fresh samples (Table 1). The procedures used for blanching (no salt) and pickling in diluted (proportion 1:4 of 100 mL) spirit vinegar (10%) were the same as described in a previous article (Drewnowska et al. 2017). The blanched and blanched and pickled mushrooms from each culinary experiment were lyophilised (model LYOVAC GT2; Steris, Germany) after draining the liquid, ground and stored in a dry condition until determination of 137 Cs and 40 K. Unprocessed subsamples of caps and stipes were sliced using a plastic knife, then lyophilised, ground to a fine powder using a porcelain mortar and pestle and divided into two halves. One half served as a control to calculate the change in activity concentrations of 137 Cs and 40 K, and the second was used in a soaking (maceration) experiment. For this, aliquots of powdered caps and stipes (ca 1 g each) in a glass beaker (100 mL) were macerated for 24 h using cooled boiled water (50 mL) at room temperature. The macerate was separated from the fungal solids after filtration through a laboratory filter paper (medium fine) under gravity. The filter and solids were lyophilised, ground, and stored in sealed polyethylene bags in dry condition. Commercially pickled samples of King Bolete, Bay Bolete, and Slippery Jack in glass jars (250 mL) were purchased randomly from retail outlets in the city of Gdańsk in Poland in 2016. These commercially pickled

Analysis
Directly before measurement of the 137 Cs and 40 K activities, the materials were deep-frozen and lyophilized for 3 days to remove any absorbed humidity. The activities were determined using a gamma spectrometer with a coaxial HPGe detector and with a relative efficiency of 18%. The resolution efficiency was 1.9 keV at 1.332 MeV (with associated electronics). The equipment was calibrated using a multi-isotope standard and the method was fully validated. The reference solution: "Standard solution of gamma emitting isotopes, code BW/Z-62/27/07" produced at the IBJ-Świerk near/Otwock in Poland, was used for preparing reference samples for equipment calibration. The same geometry of cylindrical dishes with 40 mm diameter (as applied for environmental samples) was used for reference samples during equipment calibration. Data obtained on activity concentration of 137 Cs were decay corrected back to the time of sampling. The stable K contents were calculated from the 40 K data (Falandysz et al. 2020a).

Elemental composition
In order to track changes in the activity concentrations of 137 Cs and 40 K, and the total K concentration in processed B. edulis, and to estimate hypothetical intakes with a meal, an attempt has been made to express the results both on dry and whole (wet) weight basis (Tables 1 and 2 and Appendix). When assessing the risk from contaminants accumulated in mushrooms, but also the nutritional benefits, the expression of data both on a dry and whole weight is useful to better track the change in elemental content during the course of the household treatment. Thus, in realistic approaches, the intake and exposure assessments need to relate to the whole (wet) weight mushroom meal.
B. edulis from the Tuchola Pinewoods in 2015 showed relatively low contamination with 137 Cs in the whole fruiting bodies at a level of 270 Bq kg −1 db (27 Bq kg −1 ww), while higher activity was noted for the natural radionuclide 40 K at 590 Bq kg −1 db (59 Bq kg −1 ww) (Tables 1 and 2). The mushrooms' caps usually are more contaminated with 137 Cs than stipes (Falandysz and Borovička 2013;Falandysz et al. 2018). In this study, the B. edulis was characterised by a 137 Cs activity quotient (Q C/S -of activity concentration in caps compared with stipes) of 2.8, with 2.1 to 4.5 for the cooked products on a dry biomass basis. Corresponding values for 40 K were 2.2 (2.1 to 4.1 in cooked products) (Table 1). In B. edulis the caps usually show higher concentrations of K than the stipes and the reported median Q C/S from another study was 1.5 (Frankowska et al. 2010). Radionuclide 40 K (t 1/2 is 1.248 × 10 9 years) is a minor part of the natural K that is the major metallic element in mushrooms (atomic percent occurrence is 0.0117%) (Falandysz and Borovička 2013;Falandysz et al. 2020a;Frankowska et al. 2010). Estimated total K concentration in the whole fruiting bodies of B. edulis in this study was 21,000 mg kg −1 db and 2100 mg kg −1 ww. Drying of B. edulis results in an up to tenfold increase in the content of minerals relative to the original product. In this study fresh B. edulis when blanched showed a 137 Cs activity concentration of 120 Bq kg −1 db (a decrease of 55% relative to the fresh product) equivalent to17 Bq kg −1 ww (decrease of 37%). 40 K activity was recorded at 390 Bq kg −1 db (decrease of 34%) and 54 Bq kg −1 ww (decrease of 8.5%) (Tables 1 and 2). The fresh mushrooms when blanched and pickled showed 137 Cs activity concentration of 45 Bq kg −1 db (a decrease of 83%) and 6.2 Bq kg −1 ww (decrease of 77%). 40 K activity was 77 Bq kg −1 db (a decrease of 87%) and 11 Bq kg −1 ww (decrease of 81%) (Tables 1 and 2). The total K contents in fresh B. edulis when blanched were 14,000 mg kg −1 db (1900 Bq kg −1 ww), and when blanched and pickled, were 2700 mg kg −1 db (370 mg kg −1 ww) (Appendix).
When fresh B. edulis was deep frozen for a period of one week (− 20°C) and then blanched, the 137 Cs at activity concentration was 130 Bq kg −1 db (18 Bq kg −1 ww) and the 40 K activity concentrations was 330 Bq kg −1 db (46 Bq kg −1 ww). The total K content was 8800 mg kg −1 db and 1200 mg kg −1 ww (Tables 1 and 2 and Appendix). Fresh B. edulis when deep frozen and next blanched and pickled had 137 Cs at activity concentration of 31 Bq kg −1 db (4.3 Bq kg −1 ww), and the activity of 40 K was 120 Bq kg −1 db (17 Bq kg −1 ww) (Tables 1 and 2). The total K content was 3200 mg kg −1 db (440 mg kg −1 ww) (Appendix). The 137 Cs and 40 K leaching rates from deep frozen and blanched or blanched and pickled mushrooms were 88 and 80% (db), equivalent to 84 and 72% (ww) respectively (Tables 1 and 2).
As mentioned, blanching decreases activities of 137 Cs and 40 K and contents of total K in processed mushrooms in relation to raw substrate mushrooms when the data are expressed on a dry weight (biomass) basis (Table 1). In this study the degree of reduction and hypothetical intake of the elements differed depending on whether the results were estimated on a dry biomass basis or on a whole (wet) weight. Blanched, fresh mushrooms lost 137 Cs at 55% db and depending on the morphological part, at 4 to 37% on a ww basis, while deep frozen and blanched mushrooms lost 52% db (67% ww). The loss of potassium during blanching of fresh mushrooms was 34% in db, and if expressed on a whole weight, the loss was 8.5%. When deep frozen and blanched, the reduction of K was 44% (db) and 22% (ww) ( Table 2 and Appendix).
Mushrooms collected from the wild may represent an insignificant component of the diet, but they can make a significant contribution to the intake of radiocaesium (Kiefer et al. 1965;Rantavaara 2003). Hence, cooking procedures that decrease the content of radiocaesium in mushroom are beneficial. Blanching is necessary in some cooking recipes of mushrooms. The household blanching of mushrooms retains a portion of 137 Cs within the blanched product (Tables 1 and 2) and results obtained in this study are in good agreement with the findings by Daillant et al. (2013). Frying decreases the moisture content and causes retention of a portion of 137 Cs in the cooked mushrooms, and in consequence, the fried product relative to the fresh material on a whole (wet) weight basis, can be enriched in this nuclide (Falandysz et al. 2020a, b). There is no previous data available on the reduction of potassium in mushrooms through the effects of blanching or  (Jaworska and Bernaś 2009) blanching and pickling. Activity concentration of 137 Cs in macerated mushrooms was at 14 Bq kg −1 db (1.4 Bq kg −1 ww), and the reduction in content when related to the fresh substrate was 95% (assuming 90% moisture in rehydrated product). It appears that the degree of disintegration of fruiting bodies is a major factor determining the rate at which mineral constituents leach from cells. Traditionally, the soaking period varies from 2 h to overnight (12 h) regardless of whether the powdered or sliced product is used. In practice, the rehydration yield could be < 90% if the whole dried fruiting bodies were rehydrated, due to an effect of maximal shrinkage as well as a decrease in rehydration ability in this state, while for sliced or powdered states, the rehydration yield can be higher. For comparison with other species, the fresh fruiting bodies of Cantharellus tubaeformis soaked for 12 h (200 g in 3 L fresh water) lost 40% radioactivity from 137 Cs, increasing to 50% and 61% in salted water (1% and 5% NaCl respectively) (the organoleptic values were not affected very much). The loss increased to 95% after twice rinsing and blanching, but this caused the resulting product to have a slimy consistency (Stijve 1994). Whole, dried C. tubaeformis (16 g) macerated for 30 min (0.5 L water) lost 40% of 137 Cs. However, when macerated for 15 min (0.5 L water) and then blanched for 3 min, the sample lost 99% of 137 Cs (but this procedure preserved good texture and taste in the reconstituted mushrooms) (Stijve 1994). Dried Craterellus lutescens (Fr.) Fr. (previous name Cantharellus lutescens Fr.) and Cortinarius caperatus (Pers.) Fr., (previous name Rozites caperatus (Pers.) P. Karst.) soaked in water for three hours lost 70% of 137 Cs on a dry weight biomass basis (Daillant et al. 2013). Soaking of dried shitake mushrooms in water decreased the radiocesium content by around 50% when compared with uncooked shitake (Nabeshi et al. 2013).
In this study, mushrooms after maceration, contained an activity level of 40 K at 71 Bq kg −1 db (7.1 Bq kg −1 ww) with a total K content of 2500 mg kg −1 db (250 mg kg −1 db). The rate of decrease was 88%. Results from this study confirm some findings by Daillant et al. (2013), that removal of 137 Cs using blanching and fresh boiling water is only partially successful, while on the other hand, it retains some of the potassium. Both 137 Cs and 40 K decreased more or less at a similar rate under the household processes used in this study. Decrease of 137 Cs and 40 K was roughly lower if data were calculated based on the whole (wet) weight of cooked mushrooms than on dried biomass.
Activities of 137 Cs in cooked mushrooms (potential meals) from 2015 were in the range of 1.4 to 25 Bq kg −1 ww, which is considerably lower than the maximum permitted value of 600 Bq kg −1 that is considered as a safe concentration in foodstuffs (Falandysz et al. 2020a). When considered in parallel, the activities from 40 K were in the range of 7.1 ± 3.9 to 72 ± 5 Bq kg −1 ww, i.e., 3 to 5-fold higher ( Table 2). The estimated potassium content in processed B. edulis varied from 250 ± 140 to 1900 ± 320 mg kg −1 ww, depending on the processing mode (Appendix).
If it is assumed that a 100-g whole (wet) weight portion of blanched or pickled mushrooms represents a single mushroom meal, it can provide from 25 to 460 (median 120) mg of K. This mushroom dish containing 120 mg K accounts for around 3% of the adequate daily adult intake, assuming absorption at around 90% (recommended intake is 4700 mg) (NIH 2020). Fried mushrooms on average seem to be a much better source of K intake than mushrooms that are blanched and then pickled (Falandysz et al. 2020a, b). In this study, fresh mushrooms when blanched alone could provide from 120 to 460 (median 190) mg of K in a 100-g meal. Commercially pickled B. edulis, I. badia, and S. luteus showed 137 Cs at activity concentrations of 10 ± 1.0 Bq kg −1 db, 34 ± 1.0 Bq kg −1 db and < 0.53 Bq kg −1 db, respectively. On a whole weight, the 137 Cs activity concentrations in commercially pickled products was 1.5 ± 0.1 Bq kg −1 ww in B. edulis, 4.6 ± 0.1 Bq kg −1 ww in I. badia, and < 0.07 Bq kg −1 ww in S. luteus. The moisture content of these products was in the range of 85.4 to 86.7%. Thus, the contamination levels in commercial products were much lower than those seen for B. edulis in this study. Analogically to 137 Cs, the activity concentrations from 40 K and the contents of total K in the commercial products were 50 ± 10 Bq kg −1 db and 7.3 ± 1.5 Bq kg −1 ww and 1600 ± 300 mg kg −1 db and 230 ± 50 mg kg −1 ww (B. edulis), 95 ± 11 Bq kg −1 db and 13 ± 2 Bq kg −1 ww and 3100 ± 400 mg kg −1 db and 410 ± 60 mg kg −1 ww (I. badia), and 81 ± 11 Bq kg −1 db and 11 ± 1 Bq kg −1 ww and 2600 ± 400 mg kg −1 db and 350 ± 30 mg kg −1 ww (S. luteus).

Conclusions
This study confirms earlier reports that blanching of fresh mushrooms using traditional methods of household preparation is to some degree efficient at removing 137 Cs. The initial rate of fruiting body disintegration and pre-preparation can have an impact on the leaching rate of the water-soluble fraction of metallic elements. Mushrooms that are uncontaminated or that show low concentrations of radiocaesium can still retain some potassium when subjected to blanching and pickling. Blanching of the fungal materials always decreased activities resulting from 137 Cs and 40 K, but also the total K content of the product, relative to the substrate, if data were expressed on a dry weight (biomass) basis.