¹³⁷Caesium, ⁴⁰Potassium and potassium in raw and deep-oil stir-fried mushroom meals from Yunnan in China

Highlights

• Stir-fried mushrooms showed greater contamination with ¹³⁷Cs than fresh.

• Stir-fried mushrooms on a whole weight were enriched in ¹³⁷Cs.

• Stir-fried mushrooms on a whole weight were also enriched in K and ⁴⁰K.

• A single 100 g meal provide K at 9.8–22 mg kg of body mass.

Abstract

A number of wild, edible mushroom species (Baorangia bicolor, Boletus calopus, Boletus obsclereumbrinus, Butyriboletus roseoflavus, Rubroboletus sinicus, Rugiboletus extremiorientalis and Xerocomus sp.) were collected in 2017, from Yunnan (Yuxi prefecture) in SW China. Samples of raw and stir-fried pools of these specimens were analysed for radioisotopes ¹³⁷Cs (caesium) and ⁴⁰K (potassium), and for total K concentrations. On a whole (wet) weight (ww) basis, ¹³⁷Cs activity ranged from < 0.10 to 0.75 Bq kg⁻¹ for raw, and from 0.5 to 4.4 Bq kg^-1 in stir-fried mushrooms. Radiopotassium (⁴⁰K) activity ranged from 57 to 96 Bq kg⁻¹ ww for raw, and 170 to 370 Bq kg⁻¹ ww for stir-fried mushrooms, while the corresponding concentration ranges for total K were 2100–3400 mg kg⁻¹ ww (mean: 2800 ± 3900 mg kg⁻¹ ww), and 6000–13000 mg kg⁻¹ ww-(mean: 8700 ± 2100 mg kg⁻¹ ww), respectively. This data indicates that mushrooms from this region show negligible ¹³⁷Cs contamination with evidently higher activity levels of ⁴⁰K. The deep oil stir-frying process results in enrichment in the resulting meals for all three determinants. 100 g meal portions showed ¹³⁷Cs activity in the range < 0.08 to 0.44 Bq 100 g⁻¹ ww (mean 0.15 ± 0.12 Bq 100 g⁻¹ ww), and ⁴⁰K activity from 16 to 37 Bq 100 g⁻¹ ww (mean 24 ± 6 Bq 100 g⁻¹ ww). The consequent exposure from ⁴⁰K contained in a single 100 g serving and weekly (100 g x7) servings was equivalent to radiation doses in the range of 0.099 to 0.23 μSv and 0.68–1.6 μSv per capita (means 0.15 ± 0.04 and 1.1 ± 0.3 μSv). This is equivalent to doses in the range of 0.0017 to 0.0038 μSv kg^-1 bm day^-1 and 0.011 to 0.027 μSv kg^-1 bm week^-1 respectively (mean values of 0.0025 ± 0.006 μSv kg^-1 bm day^-1and 0.018 ± 0.004 μSv kg^-1 bm week^-1). Analogically to the annual ¹³⁷Cs radiation exposure resulting from high rates of annual consumption (20–24 kg per capita), the estimated annual dose of radiation from ⁴⁰K would range from 0.34 up to 0.92 μSv kg^-1 bm (mean 0.60 μSv kg^-1 bm). Thus in practice, high annual consumption rates of wild, stir-fried mushrooms as seen in Yunnan, would result in negligible internal doses from decay of artificial ¹³⁷Cs, relative to that from natural ⁴⁰K. The 100 g servings also contained between 590–1300 mg K making this local food one of the top dietary sources of nutritionally important potassium for local consumers.

Introduction

Mushrooms are considered as a beneficial source of human dietary intake of essential inorganic macro-nutrients including potassium (K) and phosphorous (P), and micro-nutrients, e.g. zinc (Zn), copper (Cu), selenium (Se) and others, but can occasionally also be a source of some geochemical or environmental radioactive contaminants. For example, mushrooms were known as a potentially significant source of human dietary intake of radiocaesium (¹³⁷Cs) (Kiefer et al., 1965), long before the accident at the Chernobyl nuclear power plant made this contamination more widely known and led to focused studies on this pathway to human exposure (Falandysz and Borovička, 2013; Stijve and Poretti, 1990). Apart from the global atmospheric radioactive fallout from nuclear testing and the two bombs in the 1940s, major nuclear power plant disasters such as Chernobyl and Fukushima Dai-ichi in Japan also result in widespread or near-global impacts (Steinhauser et al., 2014). Recent research shows that mushrooms from all over the Chernobyl fallout zones, both proximate and more distant areas, continue to bio-accumulate ¹³⁷Cs, many years after the accident (Betti et al., 2017; Cocchi et al., 2017; Falandysz et al., 2015, 2016; Falandysz et al., 2019a; Orita et al., 2017; Türkekul et al., 2018; Vinichuk et al., 2010). The later Fukushima Daiichi incident in 2011, also caused ¹³⁷Cs contamination of foods, specifically mushrooms and game animals, in the Fukushima prefecture of Japan (Prand-Stritzko and Steinhauser, 2018), but its impact on wild mushrooms in SW China - the Yunnan and Sichuan provinces - is minor, apart from a few exceptions, possibly due to the regional climate and local weather conditions in the period following the incident (Falandysz et al., 2018; Tuo et al., 2017).

Macrofungi including the large edible species that grow in the wild, are foraged in many parts of the world and are considered to be an important source of food for local populations. Some species such as Boletus edulis and related species, Cantharellus cibarius, Tricholoma matsutake, etc., are particularly prized and are much sought after by mushroom hunters, either as a valued addition to their cuisine, or as a seasonal source of income. However, knowledge on the mineral composition of many types of edible mushrooms after culinary processing and the resulting effects on human exposure is insufficient to provide a view on this contamination pathway. This dearth of knowledge is particularly acute for certain areas, such as those that show natural geochemical soil anomalies or have suffered from particular environmental problems (Beneš et al., 2018; Borovička et al., 2014; Chiaravalle et al., 2018; Falandysz and Borovička, 2013; Falandysz et al., 2017a, 2019b and 2019c). The Yunnan province in China is a natural habitat to more than a thousand wild mushroom species with high local consumption of the edible species. Yunnan is also the main centre in China for the trading of these mushrooms collected from the wild. Thus, mushrooms may constitute a significant source of mineral macronutrients including K but, when contaminated, a potential source of dietary radiocaesium for locals who consume them regularly.

Certain local, domestic preparation procedures, e.g., washing and boiling (blanching, parboiling) but also commercial conserving procedures (pickling and canning) can substantially reduce the ¹³⁷Cs contamination levels in mushrooms. Simultaneously, these procedures can also reduce the contents of other toxic, as well as nutritionally beneficial compounds and minerals (Barnett et al., 1999; Beresford et al., 1999; Consiglio et al., 1990; Daillant et al., 2013; Drewnowska et al., 2017; Pankavec et al., 2019; Skibniewska and Smoczyński, 1999; Stijve, 1994). The reduction of ¹³⁷Cs (or any other contaminant) contents in edible fungi by cooking is thus a significant route to limiting the human intake of this radionuclide, both for mycophilous consumers as well as others who may be inadvertently exposed to contaminated fungi which form minor flavoring ingredients in mixed meals (e.g. soups, fish and meat stews).

The stir-frying of mushrooms with or without initial blanching - is typical method of cooking fresh mushrooms in China. The proportion of vegetable oil used per volume of fried mushrooms can vary depending on the particular species or on local customs or recipes.

Nevertheless, it should be mentioned that there is a huge biodiversity of edible mushrooms, as well as cooking methods and recipes (Bhatt et al., 2018; Nnorom et al., 2019; Santiago et al., 2016; Wu et al., 2019). Freshly harvested mushrooms are also eaten boiled, e.g. Macrocybe gigantea, C. cibarius and other in prepared as a soup, but are rarely eaten raw. An exceptions is freshly sliced or chipped Matsutake Tricholoma matsutake. The black Cloud ear Auricularia auricula-judae, is available dried, and is soaked before consumption, but without any thermal treatment. A large variety of dried mushrooms are available all year round in China.

When blanched -, mushrooms are known to release to varying degree, numerous organic and inorganic compounds that are highly water soluble, such as l-ascorbic acid (vitamin C), soluble proteins, soluble sugars, some colloidal constituents and metallic elements including ¹³⁷Cs and metalloids, in the usually discarded water that they are cooked in (Biekman et al., 1996; Consiglio et al., 1990; Daillant et al., 2013). Additionally, when blanched or boiled, as in a soup, mushrooms also lose their juices and dehydrate, but can simultaneously absorb the water used for cooking. Thus, immaterial to whether results are expressed on a dry biomass basis or on a whole (wet) weight basis, blanched mushrooms lose radiocesium during this cooking procedure. At the normal boiling temperature of 100 °C, the percentage loss is dependent on the blanching time, the degree of defragmentation of the fruiting bodies and possibly on the level of pre-washing (Stijve, 1994).

Mushroom preparation and cooking techniques vary but frying in oil is a popular method in many parts of the world. Stir-frying of foods using hot vegetable oil in a wok is a popular cooking method in Yunnan and elsewhere in Asia with many regional variations on the exact techniques (Qiu, 2003). There is however very little information on the effects of this mode of cooking on ¹³⁷Cs and other mineral contents of the prepared meals (Falandysz et al., 2019b; and 2019c).

A partial leakage of ¹³⁷Cs into the oil fraction has been noted when mushrooms are fried in a pan or in a flat type of vessel (Steinhauser and Steinhauser, 2016). Beresford et al. (1999) have compiled data showing that activity levels resulting from ¹³⁷Cs in fried mushrooms decrease by 50 % relative to the fresh product. An earlier study reported an even higher (70 %) rate of ¹³⁷Cs loss during frying (Kenigsberg et al., 1996), but it is unclear in both these reports as to whether the data were calculated on a whole (wet) weight or dry biomass basis. Clarification is necessary because frying in hot oil dehydrates foodstuffs, reducing the whole weight, while simultaneously preserving the mineral and contaminant contents. This often results in an apparent increase in their content in the prepared food due to the effect of concentration (Bordin et al., 2013). This study investigated the fate of ¹³⁷Cs and in parallel that of ⁴⁰K and total K, on mushrooms that were collected in the wild in the Yunnan province in China and were cooked by stir-frying using deep oil in a wok.