Radioactivity in mushrooms: A health hazard?

Food Chemistry 154 (2014) 14–25

Contents lists available at ScienceDirect

Food Chemistry journal homepage: www.elsevier.com/locate/foodchem

Review

Radioactivity in mushrooms: A health hazard? J. Guillén ⇑, A. Baeza LARUEX, Applied Physics Dept., Faculty of Veterinary Science, University of Extremadura, Avda. Universidad s/n, 10003 Cáceres, Spain

a r t i c l e

i n f o

Article history: Received 12 September 2013 Received in revised form 20 November 2013 Accepted 19 December 2013 Available online 3 January 2014 Keywords: Mushroom Radioactivity Hazard Radiocaesium Naturally occurring radionuclides Regulation

a b s t r a c t Mushrooms are a complementary foodstuff and considered to be consumed locally. The demand for mushrooms has increased in recent years, and the mushroom trade is becoming global. Mushroom origin is frequently obscured from the consumer. Mushrooms are considered excellent bioindicators of environmental pollution. The accumulation of radionuclides by mushrooms, which are then consumed by humans or livestock, can pose a radiological hazard. Many studies have addressed the radionuclide content in mushrooms, almost exclusively the radiocaesium content. There is a significant lack of data about their content from some of the main producer countries. An exhaustive review was carried out in order to identify which radionuclide might constitute a health hazard, and the factors conditioning it. Regulatory values for the different radionuclides were used. The worldwide range for radiocaesium, 226Ra, 210Pb, and 210 Po surpasses those values. Appropriate radiological protection requires that the content of those radionuclides in mushrooms should be monitored. Ó 2013 Elsevier Ltd. All rights reserved.

Contents 1. 2.

3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Radionuclide content in mushroom . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Anthropogenic radionuclides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1. Radiocaesium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.2. Radiostrontium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.3. Plutonium and americium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.4. Other anthropogenic radionuclides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Naturally occurring radionuclides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40 2.2.1. K..................................................................................................... 2.2.2. Uranium and thorium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.3. Radium, 210Pb, and 210Po . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Be . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4. Analysis of risk hazard . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Estimation of the dose by mushroom ingestion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Reduction of radionuclide content in mushrooms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Mushroom consumption, particularly that of wild mushrooms, has traditionally been considered as local. In the case of wild ⇑ Corresponding author. Tel.: +34 927257170; fax: +34 927257177. E-mail address: [email protected] (J. Guillén). 0308-8146/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodchem.2013.12.083

14 15 15 15 18 18 18 18 18 19 19 20 20 20 21 22 22 22

mushrooms, it has generally been considered that they are usually collected and consumed by the local population. This was the key factor in the successful dose reduction in areas with heavy radioactive fallout (Jacob et al., 2001; Shaw, Robinson, Holm, Frissel, & Crick, 2001). However, this local market hypothesis may no longer be valid. The demand for wild edible mushrooms has increased substantially in the last years (Voces, Díaz-Balteiro, & Alfranca,

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25

2012), and their consumption is considered a delicacy in many countries. This is reflected in a significant rise in the distribution of these products (Pettenella, Secco, & Maso, 2007). According to FAO estimates, the production of mushrooms and truffles increased steadily from 4.9  1011 kg in 1961 to a maximum of 6.4  1012 kg in 2008 (FAOSTAT, 2012). China was the main producer (more than 70% of the total production) followed by the USA, the Netherlands, Poland, and Spain (FAOSTAT, 2012). The mushroom trade is becoming global. In 2011, Spain’s exports and imports to and from other EU countries were 1.8  1010 and 2.4  1011 kg, respectively, mainly canned and preserved (Cámaras de Comercio, 2012). A negative aspect of trade in mushrooms is the usual lack of transparency of value chain traceability, although some efforts have been made to improve it (Voces et al., 2012). This global market implies that, in general, the consumer is unaware of the product’s origin (Voces et al., 2012). Mushrooms are considered excellent bioindicators of environmental pollution, since they are known to bioaccumulate heavy metals. The necessary estimation of their toxicological risk is often hindered by the lack of available data (Kalacˇ, 2010). Most radionuclides, whether anthropogenic or naturally occurring, are also heavy metals, and can be bioaccumulated by mushrooms. Their contents in mushrooms can pose a health hazard, as has occurred in areas heavily contaminated by radioactive fallout (e.g., those affected by the Chernobyl accident) since they are higher than in other foodstuffs, in particular forest products such as bilberries (Horyna, 1991; IAEA, 2006; Mietelski & Jasinska, 1996; Skuterud, Travnikova, Balonov, Strand, & Howard, 1997). In areas affected by the Chernobyl fallout, the consumption of wild mushrooms led to increased body content of radiocaesium in the population, which also showed a seasonal trend linked to the fructification of mushrooms, being higher in autumn (Shutov et al., 1996; Skuterud et al., 1997). The initial recommendation to prohibit their consumption was one of the most successful actions reducing the received dose by the population in areas with significant Chernobyl fallout (Jacob et al., 2001; Shaw et al., 2001). Likewise, the consumption and distribution of log-cultivated shiitake mushrooms (Lentinula edodes) were restricted in areas affected by the Fukushima accident (MAFF, 2012). These restraints were lifted when the mushrooms’ radioactive contents fell below regulatory values (MAFF, 2012; Hamada & Ogino, 2012). Another indirect pathway which can affect the human population, especially critical groups in the Arctic, is the consumption of game (Strand et al., 2002). Reindeer and caribou eat mushrooms whenever available. Indeed, a rumen content of up to 20% of mushrooms has been reported in an individual moose (Johanson, Bergström, Eriksson, & Erixon, 1994). Abundant spores of Xerocomus spp. and Hypholoma capnoides fungi and increased 137Cs content have been observed in the faeces of roe deer (Strandberg, 1994a). In some countries, this lead to a significant, highly seasonal, enhancement of the radiocaesium content in game meat, with maxima in the second half of the year (Hove, Pedersen, Garmo, Solheim, & Staaland, 1990; Zibold, Drissner, Kaminski, Klemt, & Miller, 2001). The analysis of the radioactive content of mushrooms has mainly focused on radiocaesium. There are essentially two reasons for this. One is that it is a long-lived anthropogenic radionuclide (T½ = 30.2 y) that has been released into the environment by atmospheric nuclear weapons tests and various accidents involving nuclear materials (UNSCEAR, 2000). The second is that it is a chemical analogue of potassium. Other anthropogenic (90Sr, 239+240Pu, 241 Am, etc.) and naturally occurring (40K, and members of the natural uranium and thorium series, among others) radionuclides have been less studied, even though their content and radiological impact can on occasions surpass those of radiocaesium (Guillén, Baeza, Ontalba, & Míguez, 2009; Vaarama, Solatie, & Aro, 2009).

15

The main objective of the present work was to estimate the anthropogenic and naturally occurring radionuclide content of mushrooms, in order to assess whether they may pose a health hazard. This content depends on several parameters, including the level of radioactive fallout or naturally occurring radionuclides in the environment, the mushroom species, its nutritional mechanism, mycelium depth, climate, bioavailability of the radionuclide, etc. According to estimates made mainly from the radiocaesium content, its contribution to the internal dose may be significant in some producing areas. However, other radionuclides with greater radiotoxicity, in particular 210Pb and 210Po, can also contribute to the internal dose (Guillén, Baeza, Ontalba, et al., 2009; Vaarama et al., 2009). The current legislation is also reviewed in order to assure the correct protection of the population, which is especially important taking into account the global market. 2. Radionuclide content in mushroom Table 1 lists the range of anthropogenic and naturally occurring radionuclides in mushrooms collected worldwide as reported in the literature. These determinations of the radioactive content of mushrooms have focused mainly on anthropogenic radionuclides as biomonitors of the radiological status of the environment. Among them, radiocaesium is the most analysed in mushrooms, mainly because of its environmental significance. The determination of other a- and/or b-emitter contents in mushrooms has been less frequent, reflecting in part the long and costly radiochemical procedures associated with their determination, even though these radionuclides can also be major contributors to the internal dose. 2.1. Anthropogenic radionuclides 2.1.1. Radiocaesium The range of variation of radiocaesium content in mushrooms worldwide after 1986 is huge – about nine orders of magnitude (Table 1). Table 2 summarizes the range of 137Cs (expressed as Bq/kg d.w.) reported in the literature for many countries, and the species which presented the highest activity levels. Data from the Fukushima accident were not included in the table since they were not as yet readily available in the literature. Also noteworthy is the almost complete absence of data, or at least of readily available data in the literature, from China, the world’s principal mushroom producer, as well as from other non-European countries among the top 20 producers (FAOSTAT, 2012). As well as 137Cs, 134 Cs was also released into the environment. However, this radionuclide is not included in Table 2, because it has a shorter half-life (T½ = 2.06 y) than 137Cs (T½ = 30.1 y), and the 134Cs/137Cs ratio is indicative of the different releases that have occurred. Indeed, 134 Cs has only been reported for countries affected by a relative recent deposition of radionuclides, such as Chernobyl or Fukushima, while it is absent from those affected by older depositions, such as global fallout in the case of Spain. There are several factors affecting the radiocaesium content in mushrooms. First, the quantity deposited onto soil is closely related to the range of the contents, especially to the maximum content. The countries seriously affected by the Chernobyl fallout (UNSCEAR, 2000) presented the highest content. The Chernobyl fallout was inhomogeneous all over the countries affected. Therefore, areas with different radioactive contamination can be found within a given country (Mietelski, Jasinska, Kozak, & Ochab, 1996; UNSCEAR, 2000). If mushrooms collected within the same local area or forest are considered, the range of variation is reduced to 1–3 orders of magnitude (Gentili, Grenigini, & Sabbatini, 1991; Mietelski, Jasinska, Kubica, Kozak, & Macharski, 1994; Mietelski, Dubchak, Blazec, Anielska, & Turnau, 2010). The maximum content

16

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25

Table 1 Range of the content of anthropogenic and naturally occurring radionuclides in fruiting bodies of fungi harvested in different countries. The data, which were reported as Bq/kg f.w., were corrected by assuming a dry/wet ratio of 0.1. Radionuclide Anthropogenic radionuclides Csa

137

90

Sr

238,239+240

241

Am

110m

125

103

Pu

Ag

Sb

Ru

131

I

Range (Bq/ Countries kg d.w.)

References

0.4– See Table 2 50,700,000 0.25–1500 Germany, Poland, Spain, Ukraine

See Table 2

0.0009– 82.8

Finland, Poland, Spain, Ukraine

0.0054– 0.067 1.5–1872

Finland, Spain

130– 10310 10–1480

Ukraine

11–48

Italy

Hungary, Italy, Slovenia

Austria, Italy

Mascanzoni (1991), Römmelt et al. (1991), Paniagua (1991), Mietelski, LaRosa, and Ghods, (1993), Romeo and Signore (1994), Lux et al. (1995), Baeza and Guillén (2004), Baeza, Guillén, Mietelski et al. (2006) Mietelski et al. (1993), Lux et al. (1995), Yamamoto et al. (1995), Mietelski et al. (2002), Outola (2003), Baeza, Guillén et al. (2004), Baeza, Guillén, Mietelski et al. (2006), Baeza, Guillén, Salas, et al. (2006), Lehto, Vaarama, and Leskinen (2013) Outola (2003), Baeza, Guillén et al. (2004), Baeza and Guillén (2006)ª, Lehto et al. (2013) Byrne (1988), Battiston et al. (1989), Gentili et al. (1991), Vaszari, Tóth, and Tarján (1992) Lux et al. (1995) Teherani (1987), Battiston et al. (1989), Romeo and Signore (1994) Romeo and Signore (1994)

Naturally Occurring Radionuclides 40 K 70–3520

234,235,236,238

228,230,232

226

Ra

210

Pb

210

Po

7

Be

Th

U

Austria, Belgium, Brazil, Bulgaria, Czech Republic , France, Bem et al. (1990), Borio et al. (1991), Gentili et al. (1991), Germany, Hungary, Ireland, Italy, Japan, Lithuania, Mexico, Muramatsu et al. (1991), Paniagua (1991), Heinrich (1993), Norway, Poland, Romania, Russia, Spain, Taiwan, Ukraine Romeo and Signore (1994), Yoshida and Muramatsu (1994a), Gaso, Cervantes, Segovia, and Salazar (1996), Calmet, Boursier, Bouisset, Guiard, and Barker (1998), Wang, Wang, Lai, & Lin (1998), Kalacˇ (2001), Ban-Nai, Muramatsu, and Yoshida (2004), Baeza, Hernández et al. (2004), Kuwahara et al. (2005), Gaso et al. (2007), Szántó, Hult, Wäjten, and Altzitzoglou (2007), Mietelski et al. (2010), Castro et al. (2012), Gwynn et al. (2013) 0.0011– Czech Republic, Germany, Poland, Spain, Ukraine, former Yamamoto et al. (1995), Mietelski et al. (2002), Wichterey 259 Yugoslavia and Sawallisch (2002), Baeza et al. (2004), Jia et al. (2004), Baeza and Guillén (2006), Baeza, Guillén, Salas et al. (2006), Zˇunic´ et al. (2008), Campos and Tejera (2010), Borovicˇka et al. (2011b) 0.0008–13 Czech Republic, Poland, Spain Mietelski et al. (2002), Baeza, Guillén et al. (2004), Baeza and Guillén (2006), Baeza, Guillén, Salas et al. (2006), Campos and Tejera (2010)b, Borovicˇka et al. (2011)b 0.021–512 Brazil, France, Germany, Spain, Ukraine Paniagua (1991), Yamamoto et al. (1995), Kirchner and Daillant (1998), Wichterey and Sawallisch (2002), Baeza, Hernández et al. (2004), Baeza, Guillén, Salas et al. (2006), Guillén Baeza, Ontalba et al. (2009), Castro et al. (2012) 0.75–289 Finland, France, Germany, Norway, Poland, Spain Kirchner and Daillant (1998), Wichterey and Sawallisch (2002), Malinowska et al. (2006), Vaarama et al. (2009), Guillén, Baeza, Ontalba, et al. (2009), Guillén, Baeza, and García (2009), Gwynn et al. (2013) 2.22–1174 Finland, Germany, Norway, Poland, Spain Wichterey and Sawallisch (2002), Skwarzec and Jakusik (2003), Guillén, Baeza, and García (2009), Vaarama et al. (2009), Gwynn et al. (2013) 1.5–380 Finland, Spain Paniagua (1991), Baeza, Hernández et al. (2004), Lönnroth et al. (2011)

a

Data from the Fukushima accident are not included. The uranium and thorium contents determined by conventional methods were converted to activity levels using the factors 9.28  105 and 2.46  104 g/Bq for total uranium and thorium, respectively. b

reported in countries such as Spain affected mainly by global fallout was several orders of magnitude lower. Before 1986, the year of the Chernobyl accident, the main source of anthropogenic radionuclides was global fallout. The range of variation pre-Chernobyl was about 37–17,800 Bq/kg d.w. (Grüter, 1966; Haselwandter, 1978; Mihok, Schwartz & Wiewel, 1989; Bem, Lasota, Kusmierek, & Witusik, 1990; Kammerer, Hiersche, & Wirth, 1994). Bem et al. (1990), comparing mushrooms collected before and after 1986, observed an increase up to a factor of ten in mushrooms collected after that date. The radiocaesium content also varies from one species of mushroom to another. Those which presented the highest content in

each country are listed in Table 2. In this table, the species which appears first for a particular country relates to the highest activity level. The range of variation for a single species was from 1 to 3 orders of magnitude (Mietelski et al., 1994; Dahlberg, Nikolova, & Johanson, 1997). For Suillus variegatus, about 40% of the variation was estimated to be due to the different locations, but the other 60% could not be explained by genetic differences (Dahlberg et al., 1997). Within a given species, the radiocaesium content presents a log-normal distribution, as that reported for Xerocomus badius in Poland (Mietelski et al., 1994). Similar frequency distributions have been obtained for various mushroom species in countries not seriously affected by the Chernobyl accident, i.e.,

Table 2 Range of 137Cs content in mushrooms after 1986 (Chernobyl accident), expressed in Bq/kg d.w., in different countries worldwide, along with the species showing the greatest accumulations of radiocaesium and the corresponding literature references. Mushroom species are ordered related to decreasing activity levels. The data reported as Bq/kg f.w. were corrected by assuming a dry/wet ratio of 0.1. Range (Bq/kg d.w.)

Species

References

EUROPE Austria Belgium

148–37370 160–102000

Bulgaria Czech Republic

41–990 50–150700

Denmark Finland

212–13343 10–121400

Xerocomus badius, Hydnum repandum, Rozites caperata Cortinarius brunneus, Cortinarius armillatus, Laccaria amethysana, Paxillus involutus Craterellus cornucopioïde, Lactarius deliciosus Laccaria amethysana, Cortinarius armillatus, Xerocomus badius Rozites caperata, Cortinarius alboviolaceus Hydnum sp., Rozites caperata

France

2.5–5595

Teherani (1987), (1988), Ismail, Dolezel, and Xarg (1995) Andolina and Guillite (1990), Fraiture, Guillitte, and Lambinon (1991), Guillite et al. (1991), Lambinon, Fraiture, Gasia, and Guillitte (1998), Szántó et al. (2007) Calmet et al. (1998), Szántó et al. (2007) Randa and Benada (1991), Cibulka et al. (1996), Calmet et al. (1998), Dvorák, Kunová, Benová, and Ohera (2006); Szántó et al. (2007) Strandberg (1994a), (1994b), (2004) Ikäheimonen, Klemola, and Ilus (2003), Kostiainen (2005), Kostiainen (2007), Lönnroth et al. (2011), Lehto et al. (2013) Calmet et al. (1998), Kirchner and Daillant (1998), Loaiza et al. (2012)

Germany

90–11290

Great Britain Hungary Italy

0.4–30500 0.6–714 95–135575

Lithuania Norway

42–3400 9–445000

Poland

40–156700

Romania Slovakia Spain Switzerland Sweden

70–360 323–966 0.5–647 3–2000 20–950000

Turkey 9.84–401 Belarus/Ukraine/Russia 9.6–50700000

Former Yugoslavia AMERICA Canada USA Mexico

a

1.5–117000 2–560 30–50 2–1521

Cantharellus sp., Rozites caperata, Xerocomus badius, Hydnum repandum Hebeloma sp., Hydnum repandum, Paxillus involutus, Rozites caperata Hydnum repandum, Boletus badius, Cantarellus cibarius Tricholoma terreum, Suillus granulatus Cantharellus lutescens, Clytocibe infandibuliformis Tricholoma equestre, Cantharellus cibarius Lactarius sp., Amanita fulva, Amanita vaginata, Cortinarius armillatus, Rozites caperata Xerocomus badius, Sarcodon imbricatum

Rückert, Diehl, and Heilgeist (1990), Römmelt et al. (1991), Heinrich (1992), Kammerer et al. (1994), Zibold et al. (2001) Barnett et al. (1999), (2001), Toal, Copplestone, Johnson, Jackson, and Jones (2002) Vaszari et al. (1992), Szántó et al. (2007) Battiston et al. (1989), Borio et al. (1991), Giovanni, Nimis, and Padovani (1991), Gentili et al. (1991), Ingrao, Belloni, and Santatoni (1992), Marzano, Bracchi, and Pizzetti (2001) Calmet et al. (1998) Hove et al. (1990); Bakken and Olsen (1991); Amundsen et al. (1996), Gwynn et al. (2013)

Bem et al. (1990), Mietelski et al. (1993), (1994), Grabowski et al. (1994), Zagrodzki, Mietelski, Krosniak, and Petelenz (1994), Mietelski et al. (1996), Pietrzak-Flis, Radwan, Rosiak, and Wirth (1996), Calmet et al. (1998), Mietelski et al. (2002), (2006), Szántó et al. (2007), Mietelski et al. (2010) Hydnum repandum, Lactarius deterrimus, Boletus sp. Calmet et al. (1998), Marzano et al. (2001), Szántó et al. (2007), Tanase, Pui, Oprea, and Popa (2009) Suillus luteus, Russula aeruginea Cipáková (2004), Dvorák, Kunová, Benová, et al. (2006) Hebeloma cylindrosporum, Lactarius deliciosus Arrondo (1988), Paniagua (1991), Baeza, Hernández, et al. (2004) Boletus edulis, Rozites caperata, Xerocamus badius Foidevaux, Dell, and Tosell (2006) Dermocybe cinnamomea, Hygrophorus sp., Rozites caperata, Mascanzoni (1991), Smith, Taylor, and Sharma (1993), (1994), Guillitte et al. (1994), Dahlberg et al. (1997), Nikolova, Russula decolorans, Suillus variegates, Cortinarius collinitus Johanson, and Dahlberg (1997), McGee et al. (2000), Andersson, Lönsjö, and Rosén (2001), Mascanzoni (2001), Rosén, Vinichuk, Nikolova, and Johanson (2011), Vinichuk, Rosén, Johanson, and Dahlberg (2011) Sarcodon scabrosus, Lepista nuda, Suillus bovinus Karadeniz and Yaprak (2007) Paxillus involutus, Xerocomus badius, Lactarius torminosus Smith et al. (1993), (1994), Hoshi et al. (1994), Tsvetnova and Shcheglov (1994), Lux et al. (1995), Mietelski et al. (2002), Travnikova et al. (2002), Vinichuk and Johansson (2003), Vinichuk, Johanson, Rosén, and Nilsson (2005), Yoshida, Muramatsu, Dvornik, Zhuchenko, and Linkov (2004), Ramzaev et al. (2006), Szántó et al. (2007) Cortinarius armillatus, Laccaria amethysana Byrne (1988), Smith et al. (1993), Vilic, Barisic, Kraljevic, and Lulic (2005)

Brazil ASIA Japana

1.45–10.6

Leucopaxillus giganteus, Laccaria laccata Armillaria gallica, Boletus edulis Clavariadelphus truncatus, Gomphus floccosus, Cortinarius caerukescens Pleurotus ostreatoroseus, Agaicus sp., Lentinula edodes

0.92–16300

Hebeloma sp.,Tricholoma flavovirens

Taiwan China

1.1–7.3 2.1

Ganoderma tsuga, Lentinula edodes Boletus sp.

Mihok et al. (1989), Smith et al. (1993), (1994) Smith et al. (1993) Gaso et al. (1996), (1998), (2000), (2007)

Muramatsu et al. (1991), Tsukada, Shibata, and Sugiyama (1998), Yoshida and Muramatsu (1994a), (1994b), (1998), Ban-Nai et al. (1997), (2004), Kuwahara et al. (2005) Wang et al. (1998) Marzano et al. (2001)

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25

Country

Castro et al. (2012)

Data from the Fukushima accident are not included.

17

18

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25

Japan and Spain (Yoshida & Muramatsu, 1994b; Baeza, Hernández, et al., 2004). In the case of X. badius and Boletus erythropus, some pigments present in the cap, derivatives of the pulvinic acid, badione A1, and norbadione A2, were found to efficiently bind potassium and caesium (Aumann, Clooth, Steffan, & Steglich, 1989). The species dependence of 137Cs accumulation includes the influence of such specific factors as the habitat of the mycelium and the type of nutritional mechanism. The habitat of the mycelium, i.e., the substrate from which the mushroom takes up nutrients together with radionuclides, has a major influence on its radiocaesium content. Cultivated mushrooms, usually grown on wood, sawdust, etc., present lower 137Cs levels than wild mushrooms, due to the lower radiocaesium contents of these substrates than those of soils (Yoshida & Muramatsu, 1994b; Ban-Nai, Muramatsu, & Yoshida, 1997). One exception to this occurred recently in areas affected by the Fukushima fallout: some L. edodes mushrooms grown outdoors on raw logs in open fields were restrained from shipment (MAFF, 2012). The radiocaesium accumulated by wild mushrooms (which usually grow in soil) presents a temporal evolution (Strandberg, 2004; Amundsen, Gulden, & Strand, 1996; Mascanzoni, 2001). It decreased for Rozites caperata and Lactarius torminosus (Amundsen et al., 1996; Strandberg, 2004), remained constant for Suillus variegatus (Mascanzoni, 2001), and increased for Cantharellus spp. (Mascanzoni, 2001). These variations reflected differences in the depth of the location of their mycelium in the soil. After radiocaesium is deposited on the surface soil, it begins to migrate downwards at speeds dependent on the soil’s characteristics (clay content, organic matter, pH, etc.) (IAEA, 2006). Those species whose mycelium is located in the surface layer of soil may show decreasing 137Cs content with time, while those with deeper mycelium may show an increasing trend (Rühm, Kammerer, Hiersche, & Wirth, 1997). The mushroom’s nutritional mechanism also plays an important role in the accumulation of radiocaesium. Mycorrhizal fungi, symbiotic with tree roots, present higher 137Cs contents than saprophytes (living on organic matter) or parasites (Guillitte, Melin, & Wallberg, 1994; Kammerer et al., 1994; Yoshida & Muramatsu, 1994b; Baeza, Hernández, et al., 2004; IAEA, 2006). The higher accumulation in mycorrhizal mushrooms is attributed to the fact that the host plant can discriminate caesium from potassium, with the fungus thus acting as a filter for the host plant (Guillitte et al., 1994; Kammerer et al., 1994). This was confirmed to some extent by radiotracer laboratory experiments, in which radiocaesium transfer to pine plantlets was reduced by symbiosis with mycorrhizal fungi (Brunner, Frey, & Riesen, 1996; Riesen & Brunne, 1996). The radiocaesium content in mushrooms is not homogeneously distributed within the organism. For ripe mushrooms, it is accumulated preferentially in the gills, followed by cap and stipe (Muramatsu, Yoshida, & Sumiya, 1991; Heinrich, 1993; Baeza, Guillén, Salas, & Manjón, 2006). For young mushrooms, the percentage of radiocaesium in the stipe is higher (Baeza, Guillén, Salas et al., 2006). The stage of maturity also affects the total radiocaesium content which is maximal at ripeness and decreases with further aging, probably due to nutrient translocation back to the mycelium (Baeza, Guillén, Salas et al., 2006). 2.1.2. Radiostrontium Another long-lived (T½ = 28.8 y) anthropogenic radionuclide released into the environment is 90Sr. It is a chemical analogue of calcium. The maximum report content and the range of variation are lower than those of radiocaesium (see Table 1), but the content also reflects the amount of the radioactive deposition. In locations close to Chernobyl, the range of the content in mushrooms was 7.8–1500 Bq/kg d.w. (Romeo, & Signore, 1994; Lux, Kammerer, Rühm, & Wirth, 1995), while in more distant countries (Poland,

Germany, and Spain) the range was lower and narrower, 0.25–6.3 Bq/kg d.w. This different behaviour is explained by the different chemical properties of the Chernobyl fallout: radiocaesium was attached to volatile particles while radiostrontium was emitted as an intermediate radionuclide, so that its transport was more limited (UNSCEAR, 2000). Paxillus involutus, Boletus edulis, Clitocybe sp., and Lactarius deliciosus were reported as having high 90Sr contents. Mushrooms accumulate 90Sr to a lesser degree than 137Cs, with the 90Sr/137Cs ratio being less than unity (range 0.001–0.70) (Mascanzoni, 1991; Baeza, Guillén, & Mietelski, 2004). The 90Sr content in mushrooms is lower than that of plants collected in the same ecosystem (Römmelt, Hiersche, Schaller, & Wirth, 1991; Lux et al., 1995). Compared to plants, the elemental composition of mushrooms is characterized by high Rb and Cs contents and low Ca and Sr contents (Yoshida & Muramatsu, 1998). Due to the paucity of 90Sr data, there has been no analysis of its dependence on the nutritional mechanism. The stage of ripeness influences the accumulation of radiostrontium in the same way as radiocaesium, although the effect is less pronounced (Baeza, Guillén, Salas et al., 2006). It also affects the distribution within the mushrooms: when the fruiting bodies are ripe, radiostrontium is detected mainly in the cap + gills rather than in the stipe (Baeza, Guillén, Salas et al., 2006). 2.1.3. Plutonium and americium The range of variation reported in the literature for plutonium and americium is about five orders of magnitude (Table 1). This reflects the differing deposition of plutonium. The contents reported in the Ukraine are in the range 2.96–82.8 Bq/kg d.w. (Lux et al., 1995; Mietelski et al., 2002), which can be attributed to plutonium attachment to refractory elements in Chernobyl fallout (UNSCEAR, 2000). The range reported in other countries (Finland, Japan, Poland, and Spain) is 0.0009–0.164 Bq/kg d.w. (Yamamoto, Shiraishi, Los, Kamarikov, & Buzinny, 1995; Mietelski et al., 2002; Baeza, Guillén et al., 2004; Baeza, Guillén, Mietelski et al., 2006). Paxillus involutus and Cantharellus cibarius presented the highest content in the Ukraine, and Hebeloma cylindrosporum and Russula cessans in Spain, the latter being mainly affected by global fallout. The distribution of plutonium within the mushroom seems to be species dependent: for cultivated Pleurotus eryngii it is mainly found in the cap + gills, while for wild Tricholoma equestre it is mainly in the stipe (Baeza, Guillén, Salas et al., 2006). The americium content in mushrooms was the lowest of all the long-lived anthropogenic radionuclides considered (Table 1). It has been reported only in Finland and Spain (Outola, 2003; Baeza, Guillén et al., 2004; Baeza, Guillén, Mietelski et al., 2006). Its origin may be attributed to global fallout since the occurrence of 241Am in Chernobyl Reactor-4 was minimal, and its parent 241Pu was attached to refractory elements (UNSCEAR, 2000). Clitocybe sp., Hebeloma cylindrosporum, and Lycoperdon perlatum were reported as presenting high contents of 241Am. 2.1.4. Other anthropogenic radionuclides Other, short-lived, radionuclides (110mAg, 125Sb, 103Ru, and 131I) were also detected in mushrooms collected just after the Chernobyl accident in affected areas (Teherani, 1987; Byrne, 1988; Battiston, Degetto, Gerbasi, & Sbrignadello, 1989; Gentili et al., 1991; Romeo & Signore, 1994; Lux et al., 1995). Their ranges of variation could be due to inhomogeneities in their deposition. 2.2. Naturally occurring radionuclides 2.2.1. 40K The radioisotope 40K (0.012% of natural potassium) is the most extensively studied of the naturally occurring radionuclides, since

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25

it is usually determined simultaneously together with radiocaesium. As potassium is an essential nutrient, its range of variation is limited – about three orders of magnitude (Table 1) – and the commonest values reported for 40K are in the range 1000–2000 Bq/kg d.w., depending on the species. The frequency distribution of 40K is of Gaussian type, unlike the log-normal distribution of radiocaesium (Mietelski et al., 1994; Baeza, Hernández, et al., 2004). Although caesium is a chemical analogue of potassium, no correlation between 137Cs and 40K has been found, suggesting different uptake mechanisms for these two elements (Mietelski et al., 1994; Baeza, Hernández, et al., 2004). No difference regarding nutritional mechanism has been reported. Mycorrhizal and saprophytic mushrooms have similar contents of 40K (Yoshida & Muramatsu, 1994a; Baeza, Hernández, et al., 2004). The distribution of 40K within the mushroom is not homogeneous, with the cap + gills presenting a higher content than the stipe (Muramatsu et al., 1991; Baeza, Guillén, Salas et al., 2006). 2.2.2. Uranium and thorium The uptake by mushrooms of uranium and thorium is lower than that of 40K, since they are not essential to the development of fungus. The range of variation reported in the literature is given in Table 1. Differences between various countries have been reported. While in Poland and the Czech Republic the range was (0.0011–0.270) and (0.0008–0.496) Bq/kg d.w. for 238U and 232Th, respectively (Mietelski et al., 2002; Borovicˇka, Kubrová, Rohovec, ˇ anda, & Dunn, 2011), the range observed in Spain was (0.120– R 47.4) and (0.061–10.7) Bq/kg d.w. for the same radionuclides (Mietelski et al., 2002; Baeza, Guillén et al., 2004; Baeza & Guillén, 2006; Campos & Tejera, 2010). Due to lack of data, no influence of nutritional mechanisms has been reported. Thorium and uranium isotopes are detected preferentially in the cap + gills (Baeza, Guillén, Salas et al., 2006). The ratios of uranium (234U/238U) and thorium (230Th/232Th) isotopes belonging to the same natural series in mushroom samples are close to unity, i.e., secular equilibrium, indicative of a single uptake route for all the uranium and thorium isotopes (Mietelski et al., 2002; Baeza, Guillén et al., 2004; Zˇunic´ et al., 2008). The presence in the environment of naturally occurring radionuclides is not usually due to accidents involving nuclear materials. However, some human activities, generally known as NORM (Naturally Occurring Radioactive Materials) (IAEA, 2003), can significantly increase the content of those radionuclides in the environment. Uranium mining is one such industry. Mushrooms can also be used as biomonitors for these naturally occurring radionuclides. For example, mushrooms that had grown on waste rock piles from uranium mining and milling were found to present a higher uranium content than those collected from unaffected regions (Wichterey & Sawallisch, 2002) or other countries (Mietelski et al., 2002; Baeza, Guillén et al., 2004; Baeza & Guillén, 2006; Campos & Tejera, 2010; Borovicˇka et al., 2011). Uranium bioaccumulation by mushrooms has been used to identify depleted uranium (DU) in areas of former Yugoslavia, where this kind of ammunition was used (Jia, Belli, Sansone, Rosamilia, & Gaudino, 2004; Zˇunic´ et al., 2008). Evidence for DU was found in only one sample in which 236U was detected (Jia et al., 2004). Tricholoma equestre, Macrolepiota procera, and C. cibarius were found to have high uranium contents (Campos & Tejera, 2010), and Lepista nuda, C. cibarius, and Clitocybe gibba high thorium contents (Campos & Tejera, 2010). 2.2.3. Radium, 210Pb, and 210Po Table 1 gives the range of radium, 210Pb, and 210Po reported in the literature. Since 226Ra, 210Pb, and 210Po belong to the same natural series (4n + 2) whose parent is 238U, mushrooms collected in the vicinity of a uranium mine were found to present higher con-

19

tents of these isotopes than those collected in unaffected areas (Wichterey & Sawallisch, 2002). Excluding areas affected by these activities, the range of variation for 226Ra is lower than that given in Table 1, i .e., 0.021–87 Bq/kg d.w. (Wichterey & Sawallisch, 2002; Baeza, Hernández, et al., 2004; Baeza & Guillén, 2006; Guillén, Baeza, Ontalba, et al., 2009; Castro, Maihara, Silva, & Figueira, 2012). Another radium isotope, 228Ra, belonging to the (4n) natural series whose parent is 232Th, was reported in Brazil within the range 6.2–54.2 Bq/kg d.w. (Castro, Maihara, Silva, & Figueira, 2012). Comparing the radium activity ranges with those of the respective parent (238U for 226Ra and 232Th for 228Ra), one observes that the maximum radium values were higher than those of the parent, suggesting that they are not in equilibrium in the mushroom. This increase in radium content might be due to the chemical similarities of calcium and radium, both alkaline-earth elements. The nutritional mechanism seemed not to influence radium uptake since, in areas unaffected by NORM activities, mycorrhizal and saprophytic species had similar activity levels (Baeza, Hernández, et al., 2004). In these areas the frequency distribution of 226Ra was symmetrical and of Gaussian type (Baeza, Hernández, et al., 2004). This radioisotope was found preferentially in the cap + gills relative to the stipes (Baeza, Guillén, Salas, et al., 2006). L. deliciosus, Lycoperdon sp., Terfezia arenaria, and Pleurotus ostreatoroseus showed high 226Ra contents (Baeza, Hernández, et al., 2004; Castro et al., 2012). The isotope 210Pb occurs as a descendant of the decay of 226Ra, but since radon is an intermediate daughter between these two radionuclides in the decay chain and is a gas, it emanates from the soil into the atmosphere. There, it decays to 210Pb which might end up as direct deposition onto the fruiting bodies. However, comparisons with the uptake of stable lead showed that mushrooms mainly take 210Pb up directly from the soil (Kirchner & Daillant, 1998). Correlations between 210Pb and stable lead have been reported, and its frequency distribution was found to be asymmetric (Guillén, Baeza, Ontalba, et al., 2009). For some species, i.e., L. deliciosus and L. perlatum, the 210Pb content was greater than that of its predecessor, 226Ra (Guillén, Baeza, Ontalba, et al., 2009), showing disequilibrium within the natural series. Fomes fomentarius, Sarcasphaera crassa, and L. perlatum presented high 210 Pb contents. Leccinum vulpilum, L. versipelle, and Suillus luteus presented high 210Po contents (Vaarama et al., 2009). The connection between the two is that 210Pb (T½ = 22.3 yr) decays to 210Bi (T½ = 5.013 d) and then to 210Po (T½ = 138.376 d). Because of this decay chain and the short half-lives of 210Bi and 210Po, any data reporting 210Po content in mushrooms should be accompanied by the corresponding 210Pb content (Guillén, Baeza, & García, 2009; Vaarama et al., 2009). Most mushrooms accumulate 210Po preferentially over 210Pb, with 210Po/210Pb ratios in the range 0.87–320 (Guillén, Baeza, & García, 2009; Vaarama et al., 2009; Gwynn, Nalbandyan, & Rudolfsen, 2013). Therefore, 210Pb and 210Po were usually not in secular equilibrium in the fruiting bodies. This might be a consequence of the greater 210Po content in the litter layer of the soil (Vaarama et al., 2009), which may be accumulated in the mycelium and translocated to the mushrooms. Further research is needed to determine whether this is the predominant pathway. The pattern of the distribution of 210Pb and 210Po within the mushrooms seems to be species dependent. In some species of the Boletaceae family, the cap content was higher than that of the stipe (Vaarama et al., 2009). The cap/stipe ratio was (0.55–2.01) and (0.64–712) for 210Pb and 210Po, respectively (Skwarzec & Jakusik, 2003; Vaarama et al., 2009). In other cases, the distribution varied with forest type for a given species (Vaarama et al., 2009), which might be attributable to the development stage of the fruiting bodies.

20

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25 Table 3 Range of annual mushroom consumption rates in different countries, expressed in kg f.w./y. Country

Consumption rate (kg f.w./y)

References

Belarus Czech Republic Finland Germany Japan Mexico Norway Poland Russia

4 5–10 0.06–1.4 0.5–16.8 3.5–4 10 0.2–58.4 10 1–20

Spain Sweden Taiwan United Kingdom Ukraine

1.3 2.8 0.09–0.26 0.06–25.68 0–18.3

Jacob et al. (2001) Horyna (1991), Kalacˇ (2010) Strand et al. (2002), Vaarama et al. (2009) Skuterud et al.) (1997), Wichterey and Sawallisch (2002) Muramatsu et al. (1991), Ban-nai et al. (2004) Gaso et al. (2007) Strand et al. (2002), Gwynn et al. (2013) Malinowska et al. (2006) Skuterud et al. (1997), Jacob et al. (2001), Travnikova et al. (2002), Strand et al. (2002), Travnikova et al. (2004), Dementyev and Bolsunovsky (2009) Requejo, Ortega, Robles, and Suáñez (2001) Strand et al. (2002) Wang et al. (1998) Barnett et al. (1999), (2001), Kalacˇ (2010) Beresford et al. (2001), Jacob et al. (2001)

2.2.4. 7Be The cosmogenic radioisotope 7Be (T½ = 53.4 d) is generated by the interaction of high energy cosmic rays with the atmosphere. Its occurrence in mushrooms is due to its deposition from the atmosphere by rainfall shortly before they are harvested (Baeza, Hernández, et al., 2004; Lönnroth, Lill, Björkholm, Haavisto, & Slotte, 2011). Its content in mushrooms differed between the two countries in which it was reported, being greater in Finland than in Spain. This may be attributable both to greater rainfall and to greater production of cosmogenic radionuclides at higher latitudes (Freely, Larswn, & Sanderson, 1988). Hygrophorus hypothejus, Russula paludosa, Hydnum rufescens, and Lactarius rufus presented the highest contents (Lönnroth et al., 2011). The nutritional mechanism influenced the 7Be content. The median and maximum values were greater for saprophytic than for mycorrhizal mushrooms (Baeza, Hernández, et al., 2004). This also reflected differences in the mycelium’s location in the soil. The mycelium of saprophytic fungi, whose nutrients come from the remains of organic matter, is generally located in the litter layers with abundant humus, normally at or very close to the surface, and 7Be is deposited almost directly onto them by rainfall. In contrast, the mycelium of mycorrhizal fungi is located in the soil layer in which the host plant root is growing, and this is normally at greater depths, so that the water from rainfall has to migrate downwards, taking more time (Baeza, Hernández, et al., 2004). 3. Analysis of risk hazard 3.1. Estimation of the dose by mushroom ingestion The analysis of the potential health hazard risk due to the consumption of mushrooms is based on estimating the effective ingestion dose Eq. (1):

D¼

X X Dj ¼ hðgÞj ðSv =BqÞ  Ae ðjÞðBq=kgf :w:Þ  mðkgf :w:Þ j

where h(g)j is the effective committed dose per unit uptake of the ingested radionuclide j for an individual belonging to age group g (ICRP, 2012), Ae(j) is the specific activity of the radionuclide j that the mushroom contains, and m is the fresh mass of the mushroom ingested per year by the standard individual. The summation extends over all radionuclides present in the mushroom. The h(g) values take into account the different decay modes for a considered radionuclide, giving information about its radiotoxicity, and also the intake pathway (ingestion in this case). The radiotoxicity of 210 Po, a pure a-emmitter, is higher than that of 137Cs, whose main emission is c after a b- decay, i.e. h(g) (210Po) > h(g) (137Cs) (see Table 5). As a way of example, the dose conversion factor, h(g), for 137 Cs intake implies that the effective dose due to the consumption of about 80 kBq is of 1 mSv. The effective dose estimate is usually carried out very conservatively, assuming the worst case scenario. In the present case, we shall assume that all species of mushroom can be considered as edible, that they are eaten raw, and that the entire radionuclide content in the mushroom can be assimilated by man. With respect to this last assumption, various radiotracer-aided studies reported that the 134,137Cs, 85Sr, and 239Pu contents in mushrooms were mainly associated with components readily assimilable by man, with only 2–6% being associated with indigestible fractions (Baeza and Guillén, 2004; Mukhopadhyay, Nag, Laskar, & Lahiri, 2007; Dementyev & Bolsunovsky, 2009). The mass of mushroom consumed is also a key factor in dose estimation. Unfortunately, since mushrooms are not a basic foodstuff, there is little data about their consumption. However, some surveys of mushroom consumption have been carried out. The ranges of consumption for different countries they report are given

Table 4 Range of the internal dose due to mushroom consumption, expressed in mSv/y, considering only the effect of the radiocaesium content.

*

ð1Þ

j

Country

Radiocaesium Dose (mSv/y)

References

Czech Republic Finland Germany Japan Mexico Poland Russia (*) Spain Taiwan United Kingdom

1.4  102 (0.016–0.14)  103 0.002–0.48 (4.0–6)  105 (0.27–8)  103 0.08 0.150 6  107–1.9  103 4.4  107 1.47  107–1.8  102

Randa and Benada (1991) Vaarama et al. (2009) Wichterey and Sawallisch (2002) Muramatsu et al. (1991), Ban-Nai et al. (2004) Gaso et al. (2000), (2007) Malinowska et al. (2006) Dementyev and Bolsunovsky (2009) Baeza, Hernández, et al. (2004) Wang et al. (1998) Barnett et al. (1999), (2001)

Mushrooms collected in areas not significantly affected by the Chernobyl accident.

21

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25

in Table 3. The consumption rate depends on the country and gastronomic tradition. There is a wide range of variation, 0–25 kg f.w./ y, so that one can not interpolate any standard value for the annual consumption rate. The effective dose estimates available in the literature considered exclusively the radiocaesium content, assuming the same conservative hypothesis (Table 4). The values for the different countries were below the recommended effect dose level of 1 mSv/y for the general public (ICRP, 2012), since their radiocaesium contents were not particularly high. The doses due to hypothetical mushroom consumption in areas severely affected by Chernobyl fallout were usually not reported because the harvesting and consumption of mushrooms were banned. Although the dose due to radiocaesium ingestion is of great importance, especially in emergencies, there are other radionuclides whose estimated doses can not be regarded as negligible. In particular, the doses of 210Pb and 210Po were about 0.010 mSv/y in Poland (Malinowska, Szefer, & Bojanowski, 2006), and 0.000027– 0.00262 mSv/y in Finland (Vaarama et al., 2009). A greater effective dose due to 210Po, 210Pb, and 40K (0.50 mSv/y) was observed for regular consumers of large amounts of mushrooms in Norway (Gwynn et al., 2013). Those values were similar to the doses due to radiocaesium. The dose due to the consumption of mushrooms grown on areas affected by NORM activities was in the range 0.002–0.48 mSv/y (Wichterey & Sawallisch, 2002), greater than the values reported for radiocaesium in Table 4. Therefore, any adequate protection of the population against the radionuclide content in mushrooms must also take the non-negligible contribution of naturally occurring radionuclides into account. The doses due to other anthropogenic radionuclides, however, are very much lower than that due to radiocaesium, at least in Spain (Baeza, Guillén et al., 2004). The harvesting and distribution of foodstuff is regulated by national and international legislation (EC, 2008; Hamada, & Ogino, 2012). The maximum radioactivity concentration levels vary from country to country. In the EU, the limit for radiocaesium (137Cs + 134Cs) was established at 600 Bq/kg for agricultural production (EC, 2008). In Japan, as a consequence of the Fukushima accident, provisional regulatory values were adopted (Hamada & Ogino, 2012). For vegetables, in which mushrooms were included, these values were 2000 Bq/kg for radioiodine, 500 Bq/kg for radiocaesium, 100 Bq/kg for uranium, and 10 Bq/kg for plutonium and other transuranic a-emitters. Although not explicitly stated, these regulatory values are to be considered as Bq/kg f.w. In order to compare them with the data in the literature, they were transformed into Bq/d.w. using a dry/wet ratio of 0.1. This ratio was based on the mean value experimentally obtained in a previous study (Baeza, Hernández, et al., 2004). This allowed potential hazards to be identified based on the same equivalent

dose produced as that of radiocaesium, which has regulatory activity levels (EC, 2008; Hamada & Ogino, 2012). The activity level of a given radionuclide, X, which produces the same dose per unit mass consumed (Sv/kg) as that of radiocaesium was estimated using Equation 2:

hðgÞð137 CsÞ  Ae ð137 CsÞ ¼ hðgÞðXÞ  Ae ðXÞ

ð2Þ

Table 5 lists the activity levels equivalent to the Japan and EU regulatory values. They were translated into Bq/kg d.w. in order to compare them with the literature values summarized in Tables 1 and 2. The maximum values reported for anthropogenic radionuclides are well below the equivalent regulatory limits except for radiocaesium. Regarding the naturally occurring radionuclides, only 226Ra, 210Pb, and 210Po presented maximum values greater than their equivalent regulatory values. Therefore, 134,137 Cs, 226Ra, 210Pb, and 210Po should be considered target radionuclides whose contents in mushroom need to be monitored, in order to ensure adequate protection of the mushroom-consuming population. In the event that they were to surpass the equivalent regulatory values, the dose by ingestion should be estimated taking into account the consumption rates for the corresponding country, and the result compared with the legislated limit. Such determinations are particularly important given the global market that trade in mushrooms is heading towards, and the public’s generally poor awareness of the origin of the mushrooms consumed. 3.2. Reduction of radionuclide content in mushrooms Despite the very conservative criteria used in the foregoing estimations of the dose by ingestion, mushrooms are not usually eaten raw. They are generally cooked and consumed immediately or preserved. Some cooking procedures can significantly reduce the radionuclide content (Table 6). That washing reduces the radiocaesium content may be attributed to the partial removal of radiocaesium-binding pigments present in the cap (Aumann et al., 1989). The addition of 2% acetic acid to dried mushrooms (Xerocomus badius, S. luteus, and Lepista saeve) exponentially reduced their 137 Cs content over a 6–48 h time span (Dvorák, Kunová, and Benová et al., 2006). Boiling also reduced the radiocaesium content. To sucessfullly reduce the effective dose, however, the cooking or pickling fluids must be discarded (Beresford et al., 2001). The use of salt also reduced the 137Cs content. The success of these procedures (pickling, boiling, and salting) are reflective of the ready availability for man of the radionuclide content of mushrooms. Drying is an ancient method of mushroom preservation, but it is the only one that increases the radionuclide content due to the loss of water. This increase was estimated to be by a factor of 10.5

Table 5 Dose coefficients h(g) for adults (>17 y in age) (ICRP, 2012), expressed in Sv/Bq, and activity levels equivalent to the radiocaesium regulatory values in Japan (500 Bq/kg f.w. = 5000 Bq/kg d.w.) and in the EU (600 Bq/kg f.w. = 6000 Bq/kg d.w.) for different radionuclides reported in the literature. A dry/wet ratio of 0.1 was assumed in order to transform Bq/ kg f.w. into Bq/kg d.w. Radionuclide

137

Cs 90 Sr 239+240

Pu Am Ag 125 Sb 103 Ru 131 I 40 K 7 Be 241

110m

*

h(g) (Sv/Bq) adults

1.3  108 2.8  108 2.5  107 2.0  107 2.8  109 1.1  109 7.3  1010 2.2  108 6.2  109 2.8  1011

Activity Limit (Bq/kg d.w.) Japan

EU

5000 2321 100* 100* 23,214 59,090 89,041 20,000* 10,483 2.32  106

6000 2785 312 390 27,857 70,909 10,6849 3545 12,581 2.79  106

Regulatory values in Japan Hamada and Ogino (2012).

Radionuclide

h(g) (Sv/Bq) adults

238

4.5  108 4.7  108 4.9  108 2.3  107 2.1  107 7.2  108 2.8  107 6.9  107 6.9  107 1.2  106

U 235 U 234 U 232 Th 230 Th 228 Th 226 Ra 228 Ra 210 Pb 210 Po

Activity Limit (Bq/kg d.w.) Japan

EU

1000* 1000* 1000* 283 310 903 232 94 94 54

1733 1660 1592 339 371 1083 279 113 113 65

22

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25

Table 6 Percentage reduction of radiocaesium content by various cooking procedures. Cooking procedure

Reduction (%)

References

Wash Boiling Salt Frying Pickling Dry then salt Parboil, salt, then soak

20 40–87 36–63 70 59–73 75 90

Kenisberg et al. (1996), Beresford et al. (2001) Kenisberg et al. (1996), Beresford et al. (2001), Kalacˇ (2010), Travnikova et al. (2002), Travnikova et al. (2004) Beresford et al. (2001), Kalacˇ (2010) Kenisberg et al. (1996) Kenisberg et al. (1996), Dvorák, Kunová, and Benová (2006) Beresford et al. (2001) Beresford et al. (2001)

(Kenisberg et al., 1996), which is consistent with the dry/wet ratio of 0.1 that we assumed in the present work. The studies of these methods of reducing the radionuclide content have mainly focused on radiocaesium. The low association of other anthropogenic radionuclides with indigestible fractions of the mushroom (Baeza and Guillén, 2004) suggests that they should also be effective against other radionuclides, although further work would be necessary to confirm this. There is another method of reducing the radionuclide content in mushrooms – time. But this would, of course, only be effective for relatively short-lived radionuclides, such as 210Po. As noted above, the 210Po/210Pb ratio in mushrooms is species dependent and in some cases greater than unity. This excess 210Po, being unsupported by the predecessor, 210 Pb, decays with its half-life (138.376 d). This implies a reduction of about 60% of the unsupported 210Po in 6 months, and 83% in a year. The lowest activity of 210Po achievable is the decay of all the unsupported 210Po when the activity levels of 210Po and 210Pb in the mushroom would be in equilibrium (i.e., the same). This passive method of waiting might be important given that 210Po is highly radiotoxic, (see h(g) values in table 5).

conservative estimates of the doses by ingestion of mushrooms. The consumption rate is highly variable however, since it depends on each country’s gastronomic and cultural traditions. One way to deal with this inconvenience is to apply regulatory values already in use in different countries (EU, Japan). These regulatory values are based mainly on radiocaesium contents and their dosimetric effects. However, other naturally occurring radionuclides, in particular, 226Ra, 210Pb, and 210Po, can also present doses per unit mass consumed that are similar or even higher than those of the regulatory values, so that these radionuclides need to be monitored in order to ensure adequate radiological protection of the general public.

Acknowledgement We are grateful to the Autonomous Government of Extremadura (Junta de Extremadura) for the financial support to the LARUEX research group (FQM001). References

4. Conclusions Mushrooms can accumulate radionuclides in the same way as they do heavy metals. While there are numerous studies in the literature dealing almost exclusively with the radiocaesium content in mushrooms, they include few from some of the main mushroom producing countries. The data available allowed the present study to establish some characteristics of its accumulation. These included the dependence on the quantity and chemical form of the radionuclide in fallout, the species dependence of its uptake which reflected the nutritional mechanisms and the depth at which the mycelium is located in the soil, and the stage of ripeness. This last factor also affected how this radionuclide is distributed within the mushroom. Knowledge of other anthropogenic radionuclides released into the environment and naturally occurring radionuclides is much poorer, since only a few works in the literature have dealt with them. The present study has therefore presented an exhaustive review of what is known about their contents worldwide. Some radionuclides have characteristics that are similar to those of radiocaesium, while others do not. Of especial importance is an awareness of the potential of mushrooms to reflect any increase in naturally occurring radionuclides in their surrounding environment as a consequence of anthropogenic activities (NORM industries). Mushroom consumption has traditionally been considered to be confined to local markets, and indeed this was the basis of dose reduction actions following the Chernobyl accident. However, with the rapid growth in production and demand, the mushroom market is fast losing its local character and becoming global, with the problem that the origin, and consequently the radioactive content of the products is generally not available to the consumer. Adequate protection of the public from the potential radiological hazard involved in consuming mushrooms has to be based on reliable,

Amundsen, I., Gulden, G., & Strand, P. (1996). Accumulation and long term behaviour of radiocaesium in Norwegian fungi. Science of the Total Environment, 184, 163–171. Andersson, I., Lönsjö, H., & Rosén, K. (2001). Long-term studies on the transfer of 137 Cs from soil to vegetation and to grazing lambs in a mountain area in northern Sweden. Journal of Environmental Radioactivity, 52, 45–66. Andolina, J., & Guillite, O. (1990). Radiocesium availability and retention sites in forest humus. In G. Desmet, P. Nassimbeni, & M. Belli (Eds.), Proceedings of CEC Workshop Transfer of radionuclides in natural and semi-natural environments (pp. 657–663). London: Elsevier Applied Science. Arrondo, E. (1988). Mediciones de radiactividad en setas de la región Vasconavarra. Revista Ibérica de Micología, 5, 45–49 (in Spanish). Aumann, D. C., Clooth, G., Steffan, B., & Steglich, W. (1989). Complexation of cesium 137 by the cap pigments of the Bay Boletus (Xerocomus badius). Angewandte Chemie International Edition in English, 28(4), 453–454. Baeza, A., Hernández, S., Guillén, F. J., Moreno, G., Manjón, J. L., & Pascual, R. (2004a). Radiocaesium and natural gamma emitters in mushrooms collected in Spain. Science of the Total Environment, 318, 59–71. Baeza, A., Guillén, J., & Mietelski, J. W. (2004b). Uptake of alpha and beta emitters by mushrooms collected and cultured in Spain. Journal of Radioanalytical and Nuclear Chemistry, 261(2), 375–380. Baeza, A., & Guillén, F. J. (2004). Dose due to mushroom ingestion in Spain. Radiation Protection Dosimetry, 111(1), 97–100. Baeza, A., Guillén, J., Mietelski, J. W., & Gaca, P. (2006). Soil-to-fungi transfer of 90Sr, 239+240 Pu, and 241Am. Radiochimica Acta, 94, 75–80. Baeza, A., & Guillén, J. (2006). Influence of the soil bioavailability of radionuclides on the transfer of uranium and thorium to mushrooms. Applied Radiation and Isotopes, 64(9), 1020–1026. Baeza, A., Guillén, F. J., Salas, A., & Manjón, J. L. (2006). Distribution of radionuclides in different parts of a mushroom: Influence of the degree of maturity. Science of the Total Environment, 359, 255–266. Bakken, L. R., & Olsen, R. A. (1991). Accumulation of radiocaesium in fruit bodies of fungi. In G. Desmet, P. Nassimbeni, & M. Belli (Eds.), Proceedings of CEC Workshop Transfer of radionuclides in natural and semi-natural environments (pp. 664–668). London: Elsevier Applied Science. Ban-Nai, T., Muramatsu, Y., & Yoshida, S. (1997). Concentrations of 137Cs and 40K in edible mushrooms collected in Japan and radiation dose due to their consumption. Health Physics, 72(3), 384–389. Ban-Nai, T., Muramatsu, Y., & Yoshida, S. (2004). Concentration of 137Cs and 40K in mushrooms consumed in Japan and radiation dose as a result of their dietary intake. Journal of Radiation Research, 45, 325–332. Barnett, C. L., Beresford, N. A., Self, P. L., Howard, B. J., Frankland, J. C., Fulker, M. J., et al. (1999). Radiocaesium activity concentrations in the fruit bodies of

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25 macrofungi in Great Britain and an assessment of dietary intake habits. Science of the Total Environment, 231, 67–83. Barnett, C. L., Beresford, N. A., Frankland, J. C., Self, P. L., Howard, B. J., & Marriott, J. V. R. (2001). Radiocaesium intake in Great Britain as a consequence of the consumption of wild fungi. Mycologist, 15(3), 98–104. Battiston, G. A., Degetto, S., Gerbasi, R., & Sbrignadello, G. (1989). Radioactivity in mushrooms in northeast Italy following the Chernobyl accident. Journal of Environmental Radioactivity, 9, 53–60. Bem, H., Lasota, W., Kus´mierek, E., & Witusik, M. (1990). Accumulation of 137Cs by mushrooms from Rogozno area of Poland over the period 1984–1988. Journal of Radioanalytical and Nuclear Chemistry, 145(1), 39–46. Beresford, N. A., Voigt, G., Wright, S. M., Howard, B. J., Bernett, C. L., Prister, B., et al. (2001). Self-help countermeasure strategies for populations living within contaminarted areas Belarus, Russia and Ukraine. Journal of Environmental Radioactivity, 56, 215–239. Borio, R., Chicchini, S., Cicioni, R., Degli Esposti, P., Rongoni, A., Sabatini, P., et al. (1991). Uptake of radiocesium by mushrooms. Science of the Total Environment, 106, 183–190. Borovicˇka, J., Kubrová, J., Rohovec, J., Rˇanda, Z., & Dunn, C. E. (2011). Uranium, thorium and rare earth elements in macrofungi: what are the genuine concentrations? Biometals, 24, 837–845. Brunner, I., Frey, B., & Riesen, T. K. (1996). Influence of ectomycorrhization and cesium/potassium ratio on uptake and localization of cesium in Norway spruce seedlings. Tree Physiology, 16, 705–711. Byrne, A. R. (1988). Radioactivity in fungi in Slovenia, Yugoslavia, following the Chernobyl Accident. Journal of Environmental Radioactivity, 6, 177–183. Calmet, D., Boursier, B., Bouisset, P., Guiard, A., & Barker, E. (1998). Mushroom as a reference material for intercomparison exercises and as bioindicator of radiocesium deposition in soil (France and Central European countries). Applied Radiation & Isotopes, 49(1–2), 19–28. Cámaras de Comercio, (2012). Base de Datos de Comercio Exterior (Spanish Foreign Trade Statistics). Available from: . [Accessed 01.05.2012]. Campos, J. A., & Tejera, N. A. (2010). Bioconcentration factors and trace elements bioaccumulation in scorocaprs of fungi collected from quartzite acidic soils. Biological Trace Element Research, 143(1), 540–554. Castro, L. P., Maihara, V. A., Silva, P. S. C., & Figueira, R. C. L. (2012). Artificial and natural radioactivity in edible mushrooms from Sao Paulo, Brazil. Journal of Environmental Radioactivity, 113, 150–154. Cibulka, J., Šišák, L., Pulkrab, K., Miholová, D., Száková, J., Fucˇíková, A., et al. (1996). Cadmium, lead, mercury and caesium levels in wild mushrooms and forest berries from different localities of the Czech Republic. Scientia Agriculturae Bohemica, 17(2), 113–129. Cˇipáková, A. (2004). 137Cs content in mushrooms from localities in eastern Slovakia. Nukleonika, 49(1), S25–S29. Dahlberg, A., Nikolova, I., & Johanson, K. J. (1997). Intraspecific variation in 137Cs in sporocarps of Suillus variegatus in seven Swedish populations. Mycological Research, 101(5), 545–551. Dementyev, D. V., & Bolsunovsky, A. Ya. (2009). Accumulation of artificial radionuclides by edible wild mushrooms and berries in the forest of the central part of Kranoyarskii Krai. Radioprotection, 44(5), 115–120. ˇ ová, K., & Ohera, M. (2006a). Radiocesium in mushrooms Dvorˇák, P., Kunová, V., Ben from selected locations in the Czech Republic and the Slovak Republic. Radiation Environmental Biophysics, 45(2), 145–151. ˇ ová, K. (2006b). Exponential drop of radiocesium Dvorˇák, P., Kunová, V., & Ben activity in mushrooms due to the effect of acetic acid. European Food Research Technology, 222, 139–143. EC, (2008). Reglamento (CE) n 733/2008 del Consejo de 15 de julio de 2008 relativo a las condiciones de importación de productos agrícolas originarios de terceros países como consecuencia del accidente ocurrido en la central nuclear de Chernobil. Diario Oficial dela Unión Europea, 30.7.2008, L201/1-7. (in Spanish). FAOSTAT, (2012). Available from: http://faostat.fao.org/site/339 Accessed 01.05.12. Fraiture, A., Guillitte, O., & Lambinon, J. (1991). Interest of fungi as bioindicators of the radiocontamination in forest ecosystems. In G. Desmet, P. Nassimbeni, & M. Belli (Eds.), Proceedings of CEC Workshop Transfer of radionuclides in natural and semi-natural environments (pp. 477–484). London: Elsevier Applied Science. Freely, H. W., Larswn, R. J., & Sanderson, C. G. (1988). Factors that cause seasonal variations in Beryllium-7 concentration in surface air. Journal of Environmental Radioactivity, 9, 223–249. Foidevaux, P., Dell, T., & Tosell, P. (2006). Radionuclides in foodstuffs and food raw material. In M. Pöschl & L. M. L. Nollet (Eds.), Radionuclide concentrations in food and the environment. USA: CRC Taylor & Fancis Group. Gaso, M. I., Cervantes, M. L., Segovia, N., & Salazar, S. (1996). Soil-fungi radiocesium transfer in forest ecosystems in Mexico. Environment International, 22(1), S365–S368. Gaso, M. I., Segovia, N., Herrera, T., Perez-Silva, E., Cervantes, M. L., Quintero, E., et al. (1998). Radiocesium accumulation in edible wild mushrooms from coniferous forests around the Nuclear Centre of Mexico. Science of the Total Environment, 223, 119–129. Gaso, M. I., Segovia, N., Morton, O., Cervantes, M. L., Godinez, L., Pea, P., et al. (2000). 137 Cs and relationships with major trace elements in edible mushrooms from México. Science of the Total Environment, 262, 73–89. Gaso, M. I., Segovia, N., Morton, O., Lopez, J. L., Machuca, A., & Hernandez, E. (2007). Radioactive and stable metal bioaccumulation, crystalline compound and siderophore detection in Clavariadelphus truncatus. Journal of Environmental Radioactivity, 97, 57–89.

23

Gentili, A., Grenigini, G., & Sabbatini, V. (1991). Ag-110m in fungi in central Italy after the Chernobyl accident. Journal of Environmental Radioactivity, 13, 75–78. Giovanni, C., Nimis, P. L., & Padovani, R. (1991). Investigations of the performance of macromycetes as bioindicators of radioactive contamination. In G. Desmet, P. Nassimbeni, & M. Belli (Eds.), Proceedings of CEC Workshop Transfer of radionuclides in natural and semi-natural environments (pp. 485–491). London: Elsevier Applied Science. Grabowski, D., Muszynski, W., Petrykowska, M., Rubel, B., Smagala, G., & Lada, W. (1994). Activity of cesium-134 and cesium-137 in game and mushrooms in Poland. Science of the Total Environment, 157, 227–229. Grüter, H. (1966). Verhalten einheimischer Pilzarten gegenüber dem Spaltproduckt Caesium-137. Zeitschrift Lebensmittel Untersuchung, 134, 173–179 (in German). Guillén, J., Baeza, A., Ontalba, M. A., & Míguez, M. P. (2009). 210Pb and stable lead content in fungi: its transfer from soil. Science of the Total Environment, 407, 4320–4326. Guillén, J., Baeza, A., & García, E., (2009b). 210Po and 210Pb in mushrooms and their contribution to the internal dose in Spain. in: Proceedings of the International Topical Conference on Po and radioactive Pb isotopes, Sevilla, Spain. Guillitte, O., Fraiture, A., & Lambinon, J. (1991). Soil-fungi radiocesium transfer in forest ecosystems. In G. Desmet, P. Nassimbeni, & M. Belli (Eds.), Proc CEC Workshop Transfer of radionuclides in natural and semi-natural environments (pp. 468–476). London: Elsevier Applied Science. Guillitte, O., Melin, J., & Wallberg, L. (1994). Biological pathways of radionuclides originating from the Chernobyl fallout in a boreal forest ecosystem. Science of the Total Environment, 157, 207–215. Gwynn, J. P., Nalbandyan, A., & Rudolfsen, G. (2013). 210Po, 210Pb, 40K and 137Cs in edible wild berries and mushrooms and ingestion doses from high consumption rates of these wild foods. Journal of Environmental Radioactivity, 116, 34–41. Hamada, N., & Ogino, H. (2012). Food safety regulations: what we learned from the Fukushima nuclear accident. Journal of Environmental Radioactivity, 111(2012), 83–89. Haselwandter, K. (1978). Accumulation of radioactive nuclide 137Cs in fruitbodies of basidiomycetes. Health Physics, 34, 713–715. Heinrich, G. (1992). Uptake and transfer factors of 137Cs by mushrooms. Radiation Environment Biophysics, 31, 39–49. Heinrich, G. (1993). Distribution of radiocesium in the different parts of mushrooms. Journal of Environmental Radioactivity, 18, 229–245. Horyna, J. (1991). Wild mushrooms – The most significant source of internal contamination. Isotopenpraxis, 27(1), 23–24. Hoshi, M., Yamamoto, M., Kawamura, H., Shinohara, K., Shibata, Y., Kozlenko, M. T., et al. (1994). Fallout radioactivity in soil and food samples in the Ukraine: Measurements of iodine, plutonium, cesium, and strontium isotopes. Health Physics, 67(2), 187–191. Hove, K., Pedersen, Ø., Garmo, T. H., Solheim, H., & Staaland, H. (1990). Fungi: a major source of radiocesium contamination of grazing rumiants in Norway. Health Physics, 59(2), 189–192. IAEA, (2003). Extent of Environmental Contamination by Naturally Occurring Radioactive Material (NORM) and Technological Options for Mitigation. IAEA Technical reports series n 419, Vienna. IAEA, (2006). Environmental consequences of the Chernobyl accident and their remediation: twenty years of experience. Report of the Chernobyl Forum Expert Group ‘Environment’. Radiological Assessment Report Series, IAEA, Vienna. ICRP, (2012). Compendium of Dose Coefficients based on ICRP Publication 60. ICRP Publication 119 Annals of ICRP, 41(Suppl.). Ikäheimonen, T.K., Klemola, S., & Ilus, E., (2003). Behaviour of gamma emitters, Sr90 and transuranic elements in forest environment. Proceedings of the International Conference on Isotopic and Nuclear Analytical Techniques for Health and Environment, IAEA, Vienna. Ingrao, G., Belloni, P., & Santatoni, G. P. (1992). Mushrooms as biological monitors of trace elements in the environment. Journal of Radioanalytical and Nuclear Chemistry, 161(1), 113–120. Ismail, S. S., Dolezel, P., & Xarg, V. (1995). 137Cs, trace and toxic elements distribution in Austrian mushrooms. Journal of Radioanalytical and Nuclear Chemistry, 200(4), 315–336. Jacob, P., Fesenko, S., Firsakova, S. K., Likhtarev, I. A., Schotola, C., Alexakhin, R. M., et al. (2001). Remediation strategies for rural territories contaminated by the Chernobyl accident. Journal of Environmental Radioactivity, 56, 51–76. Jia, G., Belli, M., Sansone, U., Rosamilia, S., & Gaudino, S. (2004). Concentration, distribution and characteristics of depleted uranium (DU) in the Kosovo ecosystem: A comparison with the uranium behaviour in the environment uncontaminated by DU. Journal of Radioanalytical and Nuclear Chemistry, 260(3), 481–494. Johanson, K. J., Bergström, R., Eriksson, O., & Erixon, A. (1994). Activity concentrations of 137Cs in moose and their forage plants in Mid-Sweden. Journal of Environmental Radioactivity, 22, 251–267. Kalacˇ, P. (2001). A review of edible mushroom radioactivity. Food Chemistry, 75, 29–35. Kalacˇ, P. (2010). Trace element contents in European species of wild growing edible mushrooms: A review for the period 2000–2009. Food Chemistry, 122, 2–15. Kammerer, L., Hiersche, L., & Wirth, E. (1994). Uptake of radiocaesium by different species of mushrooms. Journal of Environmental Radioactivity, 23, 135–150. Karadeniz, Ö., & Yaprak, G. (2007). Dynamic equilibrium of radiocesium with stable cesium within the soil-mushroom system in Turkish pine forest. Environmental Pollution, 148, 316–324. Kenisberg, J., Belli, M., Tikhomirov, F., Buglova, E., Shevchuk, V., Renaud, Ph., Maubert, H., Bruk, G., & Shutov, V., (1996). Exposures from consumption of

24

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25

forest produce. Proc. of the 1st Internacional Conference, Luxembourg, pp 271– 283. Kirchner, G., & Daillant, O. (1998). Accumulation of 210Pb, 226Ra and radioactive cesium by fungi. Science of the Total Environment, 222, 63–70. Kostiainen, E. T. (2005). Variation in 137Cs uptake of edible mushrooms. In P. Strand, P. Børretzen, & Y. Jølle (Eds.), Proceedings from the 2nd International Conference on Radioactivity in the Environment, 2–6 October 2005 (pp. 270–273). Nice, France, Østerås, Norway: Norwegian Radiation Protection Authority. Kostiainen, E. (2007). 137Cs in Finnish wild berries, mushrooms and game meat in 2000–2005. Boreal Environment Research, 12, 23–28. Kuwahara, C., Fukumoto, A., Ohsone, A., Furuya, N., Shibata, H., Sugiyama, H., et al. (2005). Accumulation of radiocesium in wild mushrooms collected from a Japanese forest and cesium uptake by microorganisms isolated from the mushroom-growing soils. Science of the Total Environment, 345, 165–173. Lambinon, J., Fraiture, A., Gasia, M.C., & Guillitte, O., (1998). La radiocontamination des champignons sauvages en Wallonie (Belgique) suite a l’accident de Tchernobyil. In.: IVe symposium international de radioecology de Cadarache. Impact des accidents d’origine nucléaire sur l’environment, Tome 2. Centre d’etudes nucléaires de Cadarache, pp E-37 – E44 (in French). Lehto, J., Vaarama, K., & Leskinen, A. (2013). 137Cs, 239,240Pu and 241Am in boreal forest soil and their transfer into wild mushrooms and berries. Journal of Environmental Radioactivity, 116, 124–132. Loaiza, P., Brudanin, V., Piquemal, F., Reyss, J.-L., Stekl, I., Warot, G., et al. (2012). Air radioactivity levels following the Fukushima reactor accident measured at the Laboratoire Souterrain de Modane, France. Journal of Environmental Radioactivity, 114, 66–70. Lönnroth, T., Lill, J.-O., Björkholm, A., Haavisto, T., & Slotte, J. M. K. (2011). Activities of the 7Be and 137Cs nuclides in mushrooms from Southern and Western Finland. Proceedings Radiochimica Acta, 1, 233–235. Lux, D., Kammerer, L., Rühm, W., & Wirth, E. (1995). Cycling of Pu, Sr, Cs, and other longliving radionuclides in forest ecoystems of the 30-km zone around Chernobyl. Science of the Total Environment, 173(174), 375–384. MAFF, (2012). Ministery of Agriculture, Forestry and Fisheries, Japan. Revised FAQ on vegetables, shiitake mushrooms, rice, milk, dairy products, meat and eggs (as of April 25) (http://www.maff.go.jp/e/quake/press_110418-5.html. Accessed 24.07.2012. Malinowska, E., Szefer, P., & Bojanowski, R. (2006). Radionuclides content in Xerocomus badius and other commercial mushrooms from several regions of Poland. Food Chemistry, 97, 19–24. Marzano, F. N., Bracchi, P. G., & Pizzetti, P. (2001). Radioactive and conventional pollulants accumulated by edible mushrooms (Boletus sp.) are useful indicators of species origin. Environment Research Section A, 85, 260–264. Mascanzoni, D. (1991). Uptake of 90Sr and 137Cs by mushrooms following the Chernobyl accident. In G. Desmet, P. Nassimbeni, & M. Belli (Eds.), Proceedings of CEC Workshop Transfer of radionuclides in natural and semi-natural environments (pp. 459–467). London: Elsevier Applied Science. Mascanzoni, D. (2001). Long-term 137Cs contamination of mushrooms following the Chernobyl fallout. Journal of Radioanalytical and Nuclear Chemistry, 249(1), 245–249. McGee, E. J., Synnott, H. J., Johanson, K. J., Fawaris, B. H., Nielsen, S. P., Horrill, A. D., et al. (2000). Chernobyl fallout in a Swedish spruce forest ecosystem. Journal of Environmental Radioactivity, 48, 59–78. Mietelski, J. W., LaRosa, J., & Ghods, A. (1993). 90Sr and 239+240Pu, 238Pu, 241Am in some samples of mushrooms and forest soil from Poland. Journal of Radioanalytical and Nuclear Chemistry, 170(1), 243–258. Mietelski, J. W., Jasin´ska, M., Kubica, B., Kozak, K., & Macharski, P. (1994). Radioactive contamination of Poslish mushrooms. Science of the Total Environment, 157, 217–226. Mietelski, J. W., & Jasin´ska, M. (1996). Radiocesium in billberries from Poland: comparison with data for mushroom samples. Journal of Radioecology, 4, 15–25. Mietelski, J. W., Jasinska, M., Kozak, K., & Ochab, E. (1996). The method of measurement used in the investigation of radioactive contamination of forests in Poland. Applied Radiation and Isotopes, 47(9/10), 1089–1095. Mietelski, J. W., Baeza, A. S., Guillen, J., Buzinny, M., Tsigankov, N., Gaca, P., et al. (2002). Plutonium and other alpha emitters in mushrooms from Poland, Spain and Ukraine. Applied Radiation & Isotopes, 56, 717–729. _ Mietelski, J. W., Dubchak, S., Błazec, S., Anielska, T., & Turnau, K. (2010). 137Cs and 40 K in fruiting bodies of different fungal species collected in a single in southern Poland. Journal of Environmental Radioactivity, 101, 706–711. Mihok Schwartz, S., & Wiewel, A. M. (1989). Bioconcentration of fallout 137Cs by fungi and read-backed voles (Clethrionomys gapperi). Health Physics, 57(6), 959–966. Mukhopadhyay, B., Nag, M., Laskar, S., & Lahiri, S. (2007). Accumulation of radiocesium by Pleurotus citrinopileatus species of edible mushroom. Journal of Radioanalytical and Nuclear Chemistry, 273(2), 415–418. Muramatsu, Y., Yoshida, S., & Sumiya, M. (1991). Concentrations of radiocesium and potassium in basidiomycetes collected in Japan. Science of the Total Environment, 105, 29–39. Nikolova, I., Johanson, K. J., & Dahlberg, A. (1997). Radiocaesium in fuitbodies and mycorrhizae in ectomycorrhizal fungi. Journal of Environmental Radioactivity, 37(1), 115–125. Outola, I. (2003). Effect of industrial pollution on the distribution of Pu and Am in soil and on soil-to-plant transfer of Pu and Am in a pine forest in SW Finland. Journal of Radioanalytical and Nuclear Chemistry, 257(2), 267–274.

Paniagua, J.M., (1991). Concentración radiactiva en suelos de la provincia de Cáceres. Modelización dosimétrica por irradiación externa. Ph Thesis, Cáceres, Spain (in Spanish). Pettenella, D., Secco, L., & Maso, D. (2007). NWFP&S marketing: lessons learned and new development paths from case studies in some European countries. SmallScale Forestry, 6, 273–390. Pietrzak-Flis, Z., Radwan, I., Rosiak, L., & Wirth, E. (1996). Migration of 137Cs in soils and its transfer to mushrooms and vascular plants. Science of the Total Environment, 186, 243–250. Ramzaev, V., Andersson, K. G., Barkovski, A., Fogh, C. L., Mishine, A., & Roed, J. (2006). Long-term stability of decontamination effect in recreational areas near the town Novozybkov, Bryansk Region, Russia. Journal of Environmental Radioactivity, 83, 280–298. ˇ Randa, Z., & Benada, J. (1991). Mushrooms – Significant source of internal contamination by radiocaesium. In G. Desmet, P. Nassimbeni, & M. Belli (Eds.), Proceedings of CEC Workshop Transfer of radionuclides in natural and seminatural environments (pp. 169–178). London: Elsevier Applied Science. Requejo, A.M., Ortega, R.M., Robles, B., & Suáñez, A., (2001). Estudio sobre dietas y hábitos alimentarios en la población española. Informe Final Convenio CSNCIEMAT, CIEMAT IAEPIRA /05/01. (in Spanish). Riesen, T., & Brunne, I. (1996). Effect of ectomycorrhizae and ammonium on 134Cs and 85Sr uptake into Picea abies seedlings. Environmental Pollution, 93(1), 1–8. Romeo, F., & Signore, A., (1994). La presenza di micro e macroelementi nei fungí: una rassegna. Rivista di Merceologia, 33(IV), 255–308 (in Italian). Römmelt, R., Hiersche, L., Schaller, G., & Wirth, E. (1991). Influence of soil fungi (basidiomycetes on the migration of Cs-134+137 and Sr-90 in coniferous forest soils. In G. Desmet, P. Nassimbeni, & M. Belli (Eds.), Proc CEC Workshop Transfer of radionuclides in natural and semi-natural environments (pp. 152–160). London: Elsevier Applied Science. Rosén, K., Vinichuk, M., Nikolova, I., & Johanson, K. (2011). Long-term effects of single potassium fertilization on 137Cs levels in plants and fungi in a boreal forest ecosystem. Journal of Environmental Radioactivity, 102, 178–184. Rückert, G., Diehl, J.F., & Heilgeist, M., (1990). Radioactivity levels in mushrooms collected in the area of Karlsruhe during 1987 and 1988. Zeitschrift fur Lebensmittel-Untersuchung und –Forschung, 190(6), 496–500. (in German). Rühm, W., Kammerer, L., Hiersche, L., & Wirth, E. (1997). The 137Cs/134Cs ratio in fungi as an indicator of the major mycelium location in forest soil. Journal of Enrivonmental Radioactivity, 35(2), 129–148. Shaw, G., Robinson, C., Holm, E., Frissel, M. J., & Crick, M. (2001). A cost-benefit analysis of long-term management options for forest following contamination with 137Cs. Journal of Environmental Radioactivity, 56, 185–2008. Shutov, V. N., Bruk, G. Ya., Basalaeva, L. N., Vasilevitsky, V. A., Ivanova, N. P., et al. (1996). The role of mushroom and berries in the formation of internal exposure doses to the population of Russia after the Chernobyl accident. Radiation Protection Dosimetry, 67(1), 55–64. Skuterud, L., Travnikova, I. G., Balonov, M. I., Strand, P., & Howard, B. J. (1997). Contribution of fungi to radiocaesium intake by rural populations in Russia. Science of the Total Environment, 193, 237–242. Skwarzec, B., & Jakusik, A. (2003). 210Po bioaccumulation by mushrooms from Poland. Journal of Environmental Monitoring, 5, 791–794. Smith, M. L., Taylor, H. W., & Sharma, H. G. (1993). Comparison of the postChernobyl 137Cs contamination of mushrooms from Eastern Europe, Sweden, and North America. Applied Environmental Microbiology, 59(1), 134–139. Smith, M. L., Taylor, H. W., & Sharma, H. D. (1994). Using c-ray spectroscopy for the study of Chernobyl fallout on edible mushrooms. Journal of Radioanalytical and Nuclear Chemistry, 180(1), 109–113. Strand, P., Howard, B. J., Aarkrog, A., Balonov, M., Tsaturov, Y., Bewerfs, J. M., et al. (2002). Radioactive contamination in the Artic - sources, dose assessments and potential risks. Journal of Environmental Radioactivity, 60, 5–21. Strandberg, M. (1994a). Mushroom spores and 137Cs in faeces of the roe deer. Journal of Environmental Radioactivity, 23, 189–203. Strandberg, M. (1994b). Radiocesium in a Danish pine forest ecosystem. Science of the Total Environment, 157, 125–132. Strandberg, M. (2004). Long-term trends in the uptake of radiocesium in Rozites caperatus. Science of the Total Environment, 327, 315–321. Szántó, Z., Hult, M., Wäjten, U., & Altzitzoglou, T. (2007). Current radioactivity content of wild edible mushrooms: a candidate for an environmental reference material. Journal of Radioanalytical and Nuclear Chemistry, 273(1), 167–170. Tanase, C., Pui, A., Oprea, A., & Popa, K. (2009). Translocation of radioactivity from substrate to macromycetes in the Crucea (Romania) unramiun mining area. Journal of Radioanalytical and Nuclear Chemistry, 281, 563–567. Teherani, D. K. (1987). Accumulation of 103Ru, 137Cs and 134Cs in fruitbodies of various mushrooms form Austria after the Chernobyl accident. Journal of Radioanalytical and Nuclear Chemistry, 117(2), 69–74. Teherani, D. K. (1988). Determination of 137Cs and 134Cs radioisotopes in various mushrooms from Austria one year after the Chernobyl incident. Journal of Radioanalytical and Nuclear Chemistry, 126(6), 401–406. Travnikova, I. G., Shutov, V. N., Bruk, G. Ya., Balonov, M. I., Skuterud, L., Strand, P., et al. (2002). Assessment of current exposure levels in different populations groups of the Kola Peninsula. Journal of Environmental Radioactivity, 60, 235–248. Travnikova, I. G., Bazjukin, A. N., Bruk, G. Ja., Shutov, V. N., Balonov, M. I., Skuterud, L., et al. (2004). Lake fish as the main contributor of internal dose to lakeshore residents in the Chernobyl contaminated area. Journal of Environmental Radioactivity, 77, 63–75.

J. Guillén, A. Baeza / Food Chemistry 154 (2014) 14–25 Tsukada, H., Shibata, H., & Sugiyama, H. (1998). Transfer of radiocaesium and stable caesium from substrata to mushrooms in a pine forest in Rokkasho-mura, Aomori. Japan. Journal of Environmental Radioactivity, 39(2), 149–160. Tsvetnova, O. B., & Shcheglov, A. I. (1994). Cs-137 content in the mushrooms of radioactive contaminated zones of the European part of the CIS. Science of the Total Environment, 155, 25–29. Toal, M. E., Copplestone, D., Johnson, M. S., Jackson, D., & Jones, S. R. (2002). Quantifying 137Cs aggragated transfer coefficients in a semi-natural woodland ecosystem adjacent to a nuclear reprocessing facility. Journal of Environmental Radioactivity, 63, 85–103. UNSCEAR, (2000). United Nations Scientific Committee on the Effects of Atomic Radiation. UNSCEAR 2000 Report to the General Assembly, with scientific annexes, New York. Vaarama, K., Solatie, D., & Aro, L. (2009). Distribution of 210Pb and 210Po concentrations in wild berries and mushrooms in boreal forest ecosystems. Science of the Total Environment, 408, 84–91. Vaszari, E. E., Tóth, V., & Tarján, S. (1992). Determination of radioactivities of some species of higher fungi. Journal of Radioanalytical and Nuclear Chemistry, 165(6), 345–350. Vilic, M., Barisic, D., Kraljevic, P., & Lulic, S. (2005). 137Cs concentration in meat of wild boars (Sus scrofa) in Croatia a decade and a half after the Chernobyl accident. Journal of Environmental Radioactivity, 81, 55–62. Vinichuk, M. M., & Johansson, K. J. (2003). Accumulation of 137Cs by fungal mycelium in forest ecosystems of Ukraine. Journal of Environmental Radioactivity, 64, 27–43. Vinichuk, M. M., Johanson, K. J., Rosén, K., & Nilsson, I. (2005). Role of the fungal mycelium in the retention of radiocaesium in forest soils. Journal of Environmental Radioactivity, 78, 77–92. Vinichuk, M., Rosén, K., Johanson, K. J., & Dahlberg, A. (2011). Correlations between potassium, rubidium and cesium (133Cs and 137Cs) in sporocarps of Suillus variegatus in a Swedish boreal forest. Journal of Environmental Radioactivity, 102, 386–392. Voces, T., Díaz-Balteiro, L., & Alfranca, O. (2012). Demand for wild edible mushrooms. The case of Lactarius deliciosus in Barcelona (Spain). Journal of Forest Economy, 18, 47–60.

25

Wang, J., Wang, C., Lai, S., & Lin, Y. (1998). Radioactivity concentrations of 137Cs and 40 K in basidiomycetes collected in Taiwan. Applied Radiation & Isotopes, 49(1–2), 29–34. Wichterey, K., & Sawallisch, S. (2002). Naturally occurring radionuclides in mushroom from uranium mining regions in Germany. Radioprotection, 37, 353–358. Yamamoto, M., Shiraishi, K., Los, I. P., Kamarikov, I. Y., & Buzinny, M. G. (1995). Alpha-emitting radionuclide content in food samples as related to the Chernobyl accident. Journal of Radioanalytical and Nuclear Chemistry, 201(6), 459–468. Yoshida, S., & Muramatsu, Y. (1994a). Acumulation of radocesium in basidiomycetes collected from Japanese forests. Science of the Total Environment, 157, 197–205. Yoshida, S., & Muramatsu, Y. (1994b). Radiocesium concentrations in mushrooms collected in Japan. Journal of Environmental Radioactivity, 22, 141–154. Yoshida, S., & Muramatsu, Y. (1998). Concentrations of alkali and alkaline earth elements in mushrooms and plants collected in a Japanese pine forest, and their relationship with 137Cs. Journal of Environmental Radioactivity, 41(2), 183–205. Yoshida, S., Muramatsu, Y., Dvornik, A. M., Zhuchenko, T. A., & Linkov, I. (2004). Equilibrium of radiocesium with stable cesium within the biological cycle of contaminated forest ecosystems. Journal of Environmental Radioactivity, 75(3), 301–313. Zagrodzki, P., Mietelski, J.W., Kros´niak, M., & Petelenz, B., (1994). Accumulation of radiocesium in forest litter and selected regions of Poland and its influence on litter-to-mushroom transfer factor. In: Kucˇera, J., Obrusník, I., & Sabbioni, E. (Eds.) Nuclear analytical methods in the life sciences, pp 273–277. Zibold, G., Drissner, J., Kaminski, S., Klemt, E., & Miller, R. (2001). Time-dependence of the radiocaesium contamination to roe deer: measurement and modelling. Journal of Environmental Radioactivity, 55, 5–27. _ Zˇunic´, Z. S., Mietelski, J. W., Błazec, S., Gaca, P., Tomankiewicz, E., Ujic´, P., et al. (2008). Tracer of DU in samples of environmental bio-monitors (non-flowering plants, fungi) and soil from target sites of the Western Balkan region. Journal of Environmental Radioactivity, 99, 1324–1328.