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Bioaccumulation of Macronutrients in Edible Mushrooms in Various Habitat Conditions of NW Poland—Role in the Human Diet
Communication

210Po and 210Pb in King Bolete (Boletus edulis) and Related Mushroom Species: Estimated Effective Radiation Dose and Geospatial Distribution in Central and Eastern Europe

1
Laboratory of Toxicology and Radiation Protection, Faculty of Chemistry, University of Gdańsk, 63 Wita Stwosza Street, 80-308 Gdańsk, Poland
2
Department of Health, Medicine and Caring Science, Division of Diagnostics and Specialist Medicine, Linköping University, 581 83 Linköping, Sweden
3
Department of Toxicology, Faculty of Pharmacy, Medical University of Łódź, 1 Muszyńskiego Street, 90-151 Łódź, Poland
*
Author to whom correspondence should be addressed.
Academic Editor: Paul B. Tchounwou
Int. J. Environ. Res. Public Health 2021, 18(18), 9573; https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph18189573
Received: 22 July 2021 / Revised: 6 September 2021 / Accepted: 9 September 2021 / Published: 11 September 2021
(This article belongs to the Special Issue Environment–Macromycetes (Fungi)–Edible Fungi)

Abstract

210Po and 210Pb occur naturally and are the most radiotoxic isotopes of the uranium (U) decay chain. Samples of Boletus edulis and related mushroom species, including B. pinophilus, B. reticulatus, B. luridus and B. impolitus, collected from Poland and Belarus were investigated for the activity concentrations of these isotopes and also for their potential health risk through adult human consumption. The results showed that spatially, the occurrence of 210Po and 210Po was heterogeneous, with activities varying from 0.91 to 4.47 Bq∙kg−1 dry biomass and from 0.82 to 5.82 Bq∙kg−1 db, respectively. Caps and stipes of the fruiting bodies showed similar levels of contamination. Consumption of boletes foraged in Poland could result in exposure to a combined radiation dose of 10 µSv∙kg−1 db from both isotopes. This dose is not significant compared to the total annual effective radiation dose of 210Po and 210Pb (54–471 µSv∙kg−1) from all sources, suggesting that these mushrooms are comparatively safe for human consumption.
Keywords: food toxicology; foodstuffs; forest; polonium; lead; radiochemistry; trace elements food toxicology; foodstuffs; forest; polonium; lead; radiochemistry; trace elements

1. Introduction

Dried mushrooms (carpophores of Basidiomycota) are relatively rich in mineral constituents (the water content of fresh mushrooms is around 90%), but radioactive elements can form a significant part of these and pose a health risk to consumers. A key example is the contamination of wild mushrooms with artificial nuclides of radiocaesium (134/137Cs) after nuclear cataclysms. These were the most commonly studied nuclides in mushrooms as documented and reviewed [1,2,3,4,5,6,7,8,9]. 210Po and its parent nuclide 210Pb originate from the 238U (uranium) decay chain. They are also the most toxic amongst the uranium chain radioactive elements, and their half-lives are 138.38 days for 210Po and 22.3 years for 210Pb [10,11,12]. 210Po, 210Pb, 226Ra and 40K as natural nuclides contribute mainly to the effective radiation background in biota that are unexposed to anthropogenic radioactivity: 210Po + 210Pb + 226Ra annually contributes 165 µSv to a daily diet, while 40K provides 140 µSv [13].
The family of the Boletus fungi is rich in genera and species that are cosmopolitan and collected worldwide [14,15]. The majority from the genus Boletus are edible (only a few are toxic, e.g., Rubroboletus satanas), tasty, and valued by local consumers. Perhaps the most remarkable and prized of these, the King Bolete, Boletus edulis, occurs relatively frequently and is native to forests of the temperate climate [14].
The objectives of this study were to evaluate the occurrence, distribution within fruiting bodies and possible risk (to consumers) from 210Po and 210Pb that tend to accumulate in Boletus edulis, Boletus pinophilus, Boletus reticulatus, Boletus luridus and Boletus impolitus mushrooms and also to prepare, based on the results, interpolation maps to spatially characterize the occurrence of both nuclides in boletes in Poland.

2. Materials and Methods

The bolete mushrooms studied, species such as B. edulis, B. pinophilus, B. reticulatus, B. luridus and B. impolitus, were collected from 25 woodlands/forested sites across Poland (the Pomerania, Kujawy, Warmia, Podlasie and Masuria regions, and the Tatra and Sudety Mts.). Also included in the study were B. reticulatus samples from two locations in Belarus (Gomel and Minsk regions) from our depository. To obtain an insight into the 210Po and 210Pb distribution within the fruitbody, some mushroom samples were separated into cap and stipe during preparation (samples/pools id. 1–17). For these, the results of 210Po and 210Pb activity concentrations in the whole specimens were calculated based on the activity concentration and biomass (caps and stipes) percentage share in the fruiting bodies (Table 1). Each analytical sample of boletes (4–5 g) had been spiked with 10 mBq of 209Po before radiochemical analysis as an internal tracer, and all prepared samples were digested using a concentrated solution (65%) of nitric acid (HNO3) [16]. The residues obtained were dissolved in 0.5M solution of HCl with added ascorbic acid. The activity concentration of 210Pb in analyzed samples was calculated indirectly via the activity measurement of its daughter 210Po. After at least six months of deposition time, the activities of the ingrown 210Po was measured in an alpha spectrometer (Canberra-Packard, USA). 210Pb activities measured in the studied boletes were calculated at their time of collection using the simplified equation for the daughter activity as a function of time [17]. The 210Po and 210Pb yield in the analyzed mushroom and soil samples ranged from 90 to 98%. The measurement results of 210Po and 210Pb activity concentrations were given with standard deviation (SD) calculated for 95% confidence intervals. The method’s accuracy was assessed using an IAEA reference material (IAEA-414) and participation in IAEA intercomparison exercises were estimated at better than 95%. Because of the abnormal distribution of radionuclides, non-parametric tests were used (U-test Mann–Whitney and H-test Kruskal–Wallis) to assess the significance of results, and the most important level achieved was quoted. Generally, the defined significance level was p = 0.05. The interpolation maps were prepared using QGIS software (QGIS Development Team) and results for the whole mushrooms.
An important aspect of chemical contaminants in biota is their uptake and distribution in the species. It has to be mentioned that the vegetative (main) body of basidiomycetes is the mycelium that is buried in the substrate, while the fruiting body (the mushroom) is an ephemeral reproductive organ used for dispersing spores into the surrounding space. Since the collection of a mycelium under natural forest conditions is generally discouraged by local customs (and regulation in some cases) because of the apparent potential damage to the habitat, it was not included in our study. Thus, to know approximately the distribution/localization of an element in a mushroom (sometimes the only cap is suitable or used for the culinary purpose) and to calculate its bioconcentration factor, a mushroom is separated into cap and stipe, which are examined individually. Therefore, it is possible to calculate, in the simplest mathematical way (no presentation of an equation/formula is necessary), the quotient of the occurrence (distribution) of an element within a specimen, expressed as the QC/S index (cap to stipe using normalized results for fully dehydrated materials).
The value of QC/S index > 1 (sometimes also called as distribution ratio, DR) shows that an element is preferentially accumulated in the caps [2,3,4,5,6,7,11,18,19]. The pattern of 210Po and 210Pb allocation in the morphological parts may change while ageing (maturing) [20], although mushrooms are generally not consumed when they reach this stage.

3. Results and Discussion

3.1. 210Po and 210Pb Activity Concentrations in Boletes

The activity concentrations determined in the bolete samples from Poland and Belarus showed a heterogeneous distribution of 210Po and 210Pb (Table 1). The activity concentrations (of 210Po and 210Pb, respectively) in whole mushrooms were in the range from 0.91 ± 0.10 Bq∙kg−1 db in Wysokie, to 4.47 ± 0.28 Bq∙kg−1 db in Osowa, and from 0.82 ± 0.09 Bq∙kg−1 db (Wysokie) to 5.82 ± 0.32 Bq∙kg−1 db (Elbląg), respectively. The results of 210Po and 210Pb activities in the Belarusian samples were similar to those in Poland (Table 1).
These activities (Table 1) were lower when compared to data reported for Boletus spp. studied in other countries. For example, 210Po and 210Pb activity concentrations in Finnish mushrooms ranged from 1.38 to 1174 ± 248 Bq∙kg−1 db; in German mushrooms, from 1.0 to 640 Bq∙kg−1 db; in Norwegian mushrooms, from 4.7 to 198 Bq∙kg−1 db; in Chinese mushrooms, from 1.66 to 308 Bq∙kg−1 db; while in other Polish species, the range was 0.23 to 36.4 Bq∙kg−1 db [12,21,22,23,24,25,26,27].
The statistical analysis showed a lack of significant differences in 210Po or 210Pb activity concentrations among the five bolete species (H-test Kruskal–Wallis p-value 0.33 for 210Po and 0.37 for 210Pb). There was also a lack of significant differences in the distribution of the nuclides between caps and stipes for each individual species and sampling point (U-test Mann–Whitney p-value 0.85 for 210Po and 0.59 for 210Pb). The bioconcentration in terrestrial species depends on the geochemical background and atmospheric fallout, but data for these parameters were not available for the boletus samples in the present study. The activities of 210Po and 210Pb in examined B. edulis, B. pinophilus, B. reticulatus, B. luridus and B. impolitus can be considered as low, suggesting that these species, similar to mushrooms of other genera from the Boletaceae family examined previously, namely the genus Leccinum and Leccinellum, do not strongly bioconcentrate 210Po and 210Pb [11,18,19]. However, again, this will depend to some extent on the background. Previously, Gwynn et al. have reported that differences in 210Po activity concentrations for individual specimens of the same mushroom species from the same stand were generally less than a factor of 3 in most cases [22].
In an attempt to visualize the spatial occurrence of 210Po and 210Pb activities in five bolete species in Poland, the activities were mapped in Figure 1 and Figure 2. 210Po mushrooms from the northern and north-eastern regions of the country (Figure 1) appeared to be more contaminated, while the occurrence of 210Pb was more heterogeneous (Figure 2). Samples collected from northern and north-eastern regions were relatively more contaminated. The 210Pb spatial occurrence was similar to that noticed earlier for the Parasol Mushroom Macrolepiota procera [28], although activity concentrations were lower in boletes. This may be explained by a number of factors, such as the natural elemental occurrence in the soil bedrock, the depth of mycelium penetration in the substrate and also by the feeding behavior and/or nuclide enrichment in the organic matter of the soil (Macrolepiota are saprophytic and favor habitats that are rich in decaying organic matter). The boletes are mutual symbionts associated with a specific plant’s rhizosphere root system, and their interactions with trees, soil substrate and soil solution are more complicated [29]. As mentioned, the levels and distribution of both 210Pb and 210Po activity concentrations in the upper soil layers can be associated not only with the parent bedrock, but to some degree also with atmospheric fallout, where they are the result of the precipitation of radon decay products from the atmosphere and the level of 210Pb and 210Po contained in the top layer of soil can be correlated with the amount of atmospheric precipitation [10,30].

3.2. Distribution of 210Po and 210Pb within a Fruitbody

Analysis of the distribution of 210Po and 210Pb within the fruiting bodies of the boletes showed a wide range of Qc/s values, i.e., 0.60–1.67 for 210Po (mean value 1.00 ± 0.19 and median 1.07 ± 0.16) and 0.55–1.52 for 210Pb (mean 0.93 ± 0.18 and median 0.93 ± 0.13). There were no statistically significant differences between concentrations in the caps and stipes (U-test Mann–Whitney p-value 0.76) (Table 2). Generally, 210Po is more mobile in soil than 210Pb and easier bioconcentrated in fruiting bodies by some Basidiomycota [12]. Lead, including 210Pb, is known to be weakly bioconcentrated by numerous Basidiomycota studied so far, while stable lead is a notorious soil pollutant because of the legacy of historical industrial pollution and also current emissions from metal (lead, copper, zinc) smelters and other use [31,32,33,34,35,36]. Thus, sometimes, a relatively elevated concentration of stable Pb observed in mushrooms is due to the high degree of substrate soil pollution [31,32,34]. This does not apply to 210Pb that typically occurs at low activity concentration levels in mushrooms, as seen in this and other studies [27,35,36,37].

3.3. Annual Effective Radiation Doses for Adults

Based on the calculated 210Po and 210Pb content in dried boletes, the effective radiation doses were estimated (in 10 kg of an equivalent fresh mushroom portion) to identify their potential radiotoxicity to consumers (Table 3).
For adults, the effective dose conversion coefficients (dose per unit exposure) for 210Po and 210Pb ingestion that ICRP recommends for the calculation of equivalent and effective doses are 1.2 and 0.69 μSv∙Bq−1, respectively [38]. In the case of the bolete samples in this study, the consumption of whole mushrooms could lead to an effective 210Po radiation dose of 1.09 ± 0.12 to 5.37 ± 0.34 μSv∙kg−1 db with a corresponding dose of 0.57 ± 0.06 to 4.02 ± 0.22 μSv∙kg−1 db from 210Pb decay.
These calculated effective radiation dose values from the samples in this study are relatively low in comparison to other regular Polish food products, such as sea fish (24.6 µSv·y−1), dietary supplements (12 µSv·y−1), fresh red currants and potatoes (3 µSv·y−1), herbal teas (6.57 µSv·y−1), stimulants such as cigarettes (471 µSv·y−1) [16,39,40,41,42,43,44,45] or other mushrooms species such as M. procera (11.62 µSv·y−1) and Leccinum spp. (14.4 μSv∙kg−1 db) [11,18,19,28,46].

4. Conclusions

This study demonstrates that B. edulis, B. pinophilus, B. reticulatus, B. luridus and B. impolitus accumulate 210Po and 210Pb at different concentrations. The interpolation maps suggest a non-uniform spatial distribution of these nuclides based on their occurrence in common edible mushrooms. The occurrence indicates the geographical distribution of these nuclides across Poland, which also shows noticeable agreement with the natural radiological background. Morphologically, the 210Po and 210Pb quotients between cap and stipe (Qc/s) ranged from 0.55 to 1.67. Consumption of the analyzed mushrooms would result in a dose of 10 µSv∙kg−1 db in total, from both 210Po and 210Pb, which would not contribute significantly to the total annual effective radiation doses from 210Po and 210Pb intake from other sources for adult consumers. This suggests that consumption of these mushrooms is comparatively safe from the radiological protection point of view.

Author Contributions

Conceptualization, D.S.-P. and J.F.; methodology, D.S.-P.; Software, G.O.; validation, A.M.; formal analysis, A.M.; investigation, A.M.; resources, D.S.-P. and J.F.; data curation, D.S.-P.; writing—original draft, D.S.-P. and G.O.; visualization, D.S.-P.; writing—review and editing, D.S.-P. and J.F.; supervision, J.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was, in some part, funded by the MINISTRY OF SCIENCES AND EDUCATION, grant number DS/531-T030-D841-21.

Institutional Review Board Statement

Not applicable—this article does not contain any studies with human participants or animals.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data supporting reported results are available on request.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Interpolation map for 210Po activity concentrations in boletes.
Figure 1. Interpolation map for 210Po activity concentrations in boletes.
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Figure 2. Interpolation map of 210Pb activity concentrations in boletes.
Figure 2. Interpolation map of 210Pb activity concentrations in boletes.
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Table 1. 210Po and 210Pb activity concentrations in boletes; a PM—Primeval Forest, b LP—Landscape Park; c210Po and 210Pb activities in whole fruiting bodies calculated based on levels in the caps and stipes and biomass share.
Table 1. 210Po and 210Pb activity concentrations in boletes; a PM—Primeval Forest, b LP—Landscape Park; c210Po and 210Pb activities in whole fruiting bodies calculated based on levels in the caps and stipes and biomass share.
NoSampling Site
(Number of Individual Specimens)
Activity Concentration (Bq·kg−1 db)
CapsStipesWhole Fruiting Bodies
210Po210Pb210Po210Pb210Po210Pb
Poland, B. edulis
1Kościerzyna (26)----1.63 ± 0.111.32 ± 0.04
2Tuchola Pinewoods (6)----1.61 ± 0.101.42 ± 0.09
3Toruńske Forest (15)----1.05 ± 0.080.99 ± 0.07
4Łukta (24)----2.15 ± 0.111.86 ± 0.06
5Puchałowo (15)----1.59 ± 0.081.32 ± 0.05
6Osowa (15)----4.47 ± 0.283.27 ± 0.23
7Olsztyn (19)----2.10 ± 0.201.74 ± 0.07
8Augustów PF a (16)----2.91 ± 0.185.28 ± 0.30
9Szczecinek (22)----1.53 ± 0.062.92 ± 0.15
10Porażyn (13)----1.13 ± 0.081.74 ± 0.10
11Mrągowo (15)----2.53 ± 0.134.76 ± 0.28
12Chochołowska Dale (12)----1.75 ± 0.112.65 ± 0.11
13Elbląg (21)----3.69 ± 0.145.82 ± 0.32
14Mojusz (11)----0.92 ± 0.071.46 ± 0.09
15Białowieża PF a (15)----2.31 ± 0.114.43 ± 0.27
16Wanacja (15)----1.54 ± 0.093.02 ± 0.14
17Goreń (15)----2.03 ± 0.093.29 ± 0.15
18Piska Wilderness (15) c1.12 ± 0.080.94 ± 0.060.75 ± 0.060.80 ± 0.050.93 ± 0.520.87 ± 0.41
19Giżycko (21) c1.15 ± 0.081.23 ± 0.091.04 ± 0.071.21 ± 0.061.10 ± 0.591.22 ± 0.60
20Seacoast LP b (9) c1.76 ± 0.101.58 ± 0.062.82 ± 0.132.94 ± 0.072.30 ± 0.862.27 ± 0.48
21Kłodzka Dale (10) c1.40 ± 0.091.22 ± 0.051.84 ± 0.131.62 ± 0.101.62 ± 0.801.42 ± 0.58
B. pinophilus
22Piska Wilderness (15) c1.52 ± 0.081.59 ± 0.081.07 ± 0.061.13 ± 0.071.30 ± 0.391.36 ± 0.44
23Noteć Forest (32) c2.38 ± 0.162.54 ± 0.141.42 ± 0.121.87 ± 0.121.89 ± 0.522.20 ± 0.47
24Wdzydze LP b (26) c1.51 ± 0.111.30 ± 0.092.25 ± 0.132.36 ± 0.141.88 ± 0.691.83 ± 0.67
25Dziemiany (14) c0.94 ± 0.081.03 ± 0.091.57 ± 0.091.96 ± 0.121.27 ± 0.271.53 ± 0.32
B. reticulatus
26Seacoast LP b (15) c4.31 ± 0.244.54 ± 0.143.24 ± 0.233.25 ± 0.133.82 ± 1.173.95 ± 0.66
B. luridus
27Wysokie (12) c0.94 ± 0.090.95 ± 0.080.86 ± 0.070.63 ± 0.090.91 ± 0.100.82 ± 0.09
28Kępice (15) c1.04 ± 0.060.98 ± 0.080.97 ± 0.071.05 ± 0.091.02 ± 0.531.00 ± 0.68
B. impolitus
29Olsztynek (15) c1.53 ± 0.111.72 ± 0.091.77 ± 0.131.66 ± 0.101.65 ± 0.681.69 ± 0.53
Belarus, B. reticulatus
30Chojniki (38) c3.18 ± 0.131.80 ± 0.122.85 ± 0.162.46 ± 0.123.03 ± 0.772.11 ± 0.62
31Borysów (34) c1.16 ± 0.071.33 ± 0.081.45 ± 0.091.63 ± 0.101.29 ± 0.391.46 ± 0.45
Table 2. Average values of the Qc/s distribution for 210Po and 210Pb in boletes.
Table 2. Average values of the Qc/s distribution for 210Po and 210Pb in boletes.
Sampling SiteDistribution (Cap/Stipe) (Qc/s)
210Po210Pb
Poland, B. edulis
Piska Wilderness1.48 ± 0.101.18 ± 0.08
Giżycko1.11 ± 0.111.01 ± 0.11
Seacoast Landscape Park0.63 ± 0.160.54 ± 0.09
Kłodzka Dale0.76 ± 0.160.75 ± 0.11
B. pinophilus
Piska Wilderness1.42 ± 0.101.41 ± 0.11
Notecka Forest1.67 ± 0.211.36 ± 0.19
Wdzydze Landscape Park0.67 ± 0.170.55 ± 0.17
Dziemiany0.60 ± 0.130.53 ± 0.15
B. reticulatus
Seacoast Landscape Park1.33 ± 0.331.40 ± 0.19
B. luridus
Wysokie1.09 ± 0.121.52 ± 0.12
Kępice1.07 ± 0.090.93 ± 0.12
B. impolitus
Olsztynek0.86 ± 0.171.04 ± 0.13
Belarus, B. reticulatus
Chojniki (BY)1.11 ± 0.200.73 ± 0.16
Borysów (BY)0.80 ± 0.110.82 ± 0.13
Mean1.00 ± 0.190.93 ± 0.18
Median1.07 ± 0.160.93 ± 0.13
Table 3. Calculated average values of the effective radiation dose for adults from 210Po and 210Pb decay through Boletus spp. consumption.
Table 3. Calculated average values of the effective radiation dose for adults from 210Po and 210Pb decay through Boletus spp. consumption.
Sampling SiteEffective Radiation Dose
(μSv·kg−1 db)
210Po210Pb
Poland, B. edulis
Pomerania, Kościerzyna1.95 ± 0.130.91 ± 0.02
Pomerania, Tuchola Pinewoods1.93 ± 0.130.98 ± 0.07
Kujawy region, Toruńskie forests1.27 ± 0.090.68 ± 0.05
Warmia, Łukta2.58 ± 0.131.28 ± 0.04
Warmia, Puchałowo1.91 ± 0.100.91 ± 0.03
Pomerania, Osowa5.37 ± 0.342.26 ± 0.16
Warmia, Olsztyn2.52 ± 0.241.20 ± 0.05
Podlasie, Augustów Primeval Forest3.49 ± 0.223.64 ± 0.21
Pomerania, Szczecinek1.84 ± 0.072.02 ± 0.10
Greater Poland, Porażyn1.35 ± 0.091.20 ± 0.07
Masuria, Mrągowo3.03 ± 0.153.28 ± 0.19
Tatra Mountains, Chochołowska Dale2.10 ± 0.141.83 ± 0.08
Warmia, Elbląg4.43 ± 0.174.02 ± 0.22
Pomerania, Mojusz1.10 ± 0.081.01 ± 0.06
Podlasie, Białowieża Primeval Forest2.78 ± 0.133.05 ± 0.18
Podlasie, Kurpiowska Forest, Wanacja1.85 ± 0.112.09 ± 0.10
Kujawy region, Goreń2.44 ± 0.102.27 ± 0.10
Masuria, Piska Wilderness1.12 ± 0.630.60 ± 0.28
Masuria, Giżycko1.32 ± 0.710.84 ± 0.41
Pomerania, Seacoast Landscape Park2.76 ± 1.031.57 ± 0.33
Sudety Mountains, Kłodzka Dale1.94 ± 0.960.98 ± 0.40
B. pinophilus
Masuria, Piska Wilderness1.56 ± 0.470.94 ± 0.30
Notecka Forests2.26 ± 0.621.52 ± 0.33
Pomerania, Wdzydze Landscape Park2.26 ± 0.831.26 ± 0.46
Pomerania, Dziemiany1.53 ± 0.321.05 ± 0.22
B. reticulatus
Pomerania, Seacoast Landscape Park4.59 ± 1.412.72 ± 0.45
B. luridus
Wysokie1.09 ± 0.120.57 ± 0.06
Pomerania, Kępice1.22 ± 0.630.69 ± 0.47
B. impolitus
Warmia, Olsztynek1.98 ± 0.811.17 ± 0.36
Belarus, B. reticulatus
Gomel region, Chojniki3.63 ± 0.921.46 ± 0.43
Minsk region, Borysów1.55 ± 0.471.01 ± 0.31
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