Toxicology & Applied Science

Toxicology & Applied Science

Neoboletus luridiformis: nutritional value, medicinal use and content of potentially toxic elements – a review and health risk assessment

Introduction

Besides constituents affecting taste, mushrooms are nutritionally desirable because of their low energy value, fibre content, specifically β-glucans, and high antioxidant capacity (Kalač, 2013). In addition, their potential medicinal use becomes increasing attention. On the other hand, the ability of some species to accumulate detrimental elements including radioisotopes has to be taken into account when considering them for regular diatry or medicinal use. This review focuses on the chemical composition, nutritional value and potential medicinal effects of Neoboletus luridiformis (see Figure 1), also known as the Scarletina bolete, previously referred to as Boletus luridiformis and sometimes mistakenly as Boletus erythropus. Moreover, the health risk arising from the potential accumulation of detrimental elements in the fruiting bodies of Neoboletus luridiformis is evaluated.

Classification and Characterization of Neoboletus luridiformis

Neoboletus luridiformis is a good edible mushroom growing in Europe and North America in similar places as B. edulis. However, it should be sufficiently cooked (20 min at least) otherwise it can cause nausea and gastric discomfort. It is a mushroom belonging to the Boletus family, which is known for producing mushrooms that feature tubes and pores underneath their caps (Kallio & Heikkila, o. J.). Neoboletus luridiformis is characterized by its brown cap, a yellowish-green tube base with orange-red pores that become rusty with age, and bruise blue to black. Its stem is yellow with dense red dots, and its yellow flesh rapidly turns deep blue when injured.

As the basis for the color reaction, variegate acid, the yellow primary dye of N. luridiformis, has been identified. Upon injury, variegate acid contained in the fruit body of the mushroom is oxidized by atmospheric oxygen with the help of oxidases to a hydroxyquinone methide, the anion of which causes the blue coloration (Steglich, 1975). The red pigment of Neoboletus luridiformis has been identified as variegatorubin, which can be obtained in vitro by oxidizing variegate acid with copper(II)acetate in acetic acid (Steglich, 1975).

Chemical composition and nutritional value

The dry matter (DM) content of both wild and cultivated mushrooms is quite low, typically ranging between 80 and 140 grams per kilogram. When the exact DM content is unknown, a standard value of 100 grams per kilogram is used for calculations. For Neoboletus luridiformis a dry matter of content of 116.4 g/kg can be found in literature (Kalač, 2013).

In a study assessing the nutritional value of five saprotrophic and five mycorrhizal wild growing mushrooms (Grangeia et al., 2011), Neoboletus luridiformis was among the mushrooms with the highest antioxidant potential, mainly due to the contribution of polar antioxidants such as phenolics and sugars. On average, mycorrhizal species, to which Neoboletus luridiformis belongs, revealed higher sugar concentrations (16-42 g/100 g dw) than assessed saprotrophic mushrooms (0.4-15 g/100 g). Furthermore, fructose was exclusively found in mycorrhizal species, ranging from 0.2 to 2.3 g per 100g of dry weight. Neoboletus luridiformis specifically contained 1.72 ± 0.03 g fructose per 100g of dry weight. Additionally, it was among the mushrooms with the highest levels of total sugars (34.46 g/100 g dw). Included among detected sugars was also trehalose with a concentration of 4.84 mg per 100 grams of dry weight. Trehalose is a disaccharide (composed of two glucose molecules bound by an alpha, alpha-1,1 linkage, with no reducing power) and is known to be one of the sources of energy in most living organisms and can be found in bacteria, fungi, insects, plants, and invertebrates. Furthermore, trehalose protects organisms against various stresses, such as dryness, freezing, and osmopressure. It has good stabilizing functions, namely, preventing starch retrogradation, protein denaturation, and lipid degradation. This saccharide shows good sweetness like sucrose, and is used in the food industry as a sweetener (Higashiyama, 2002). Mannitol content has been observed to be generally higher in mycorrhizal species compared to saprophytic species. In Neoboletus luridiformis, the mannitol level was found to be 27.90 ± 0.30 g per 100g of dry weight. Among the assessed mushrooms, Neoboletus luridiformis was found to have the lowest level of total tocopherols, with a content of 19.16 ± 2.27 g per 100g of dry weight. Neoboletus luridiformis has been further recognized as an ideal choice of wild mushroom for low-calorie diets due to its minimal fat content, measuring just 3.06g per 100g of dry weight in the study conducted by Grangeia and colleagues (Grangeia et al., 2011). The unsaturated fatty acids, oleic and linoleic acid have been reported as its most abundant fatty acids. In another study assessing the non-polar lipid content of mushrooms of the Boletaceae family (Pedneault, Karine et al., 2006), the non-polar lipid content of Neoboletus luridiformis was found to be 2.0 weight percentage [%(w/w)] of dry weight.  Similar to the study conducted by Grangeia and colleagues, oleic and linoleic fatty acids have been identified as the most abundant fatty acids, making up 18% and 63%, respectively, of the total fatty acids. In the study of Grangeia and colleagues (Grangeia et al., 2011), Neoboletus luridiformis, further revealed one of the highest radical scavenging effects, correlating with its high concentrations of polar antioxidants such as phenolics and sugars. Similarly, Boletus luridiformis demonstrated exceptional reducing power and revealed the highest percentage of lipid peroxidation inhibition among the mushrooms assessed.

Potential medicinal use and effects on human health

Mushrooms have been used since 1,000 of years in traditional medicine for several diseases and presently continue to play an important role in the discovery of new molecules (Jain et al., 2010). Mushrooms contain a multiplicity of bioactive compounds with chemical and structural variation that make them versatile in terms of biological activities (Garcia et al., 2022). Indeed, an outstanding amount of antimicrobial has been obtained from natural sources including mushrooms (M. Alves et al., 2012).

Resistance to antimicrobials and particularly multidrug-resistant bacteria represents an important public health problem and studies suggest that infections by multidrug-resistant bacteria strains are one of the major causes of morbidity and mortality worldwide (Levin-Reisman et al., 2017; Medina & Pieper, 2016). This has prompted a search for alternatives therapeutic approaches to conventional antibiotic that allow to overcome the problem of bacterial resistance (Alaoui Mdarhri et al., 2022). Moreover, the recognized safe status of natural products, has led to an increased interest in antimicrobials derived from nature (Gupta & Birdi, 2017). In this context, the attention on mushroom extracts as promising agents with antibacterial and antibiofilm activities has been revived. In fact, mushroom species are known to contain several bioactive compounds, namely phenolic acids, terpenoids, flavonoids, tannins, alkaloids, and polysaccharides that have the potential to be applied as novel and effective antibiotics (M. Alves et al., 2012).  A study by Garcia et al. which screened the antimicrobial activity of Neoboletus luridiformis water and methanol extracts against Gram-positive and Gram-negative bacteria, revealed antimicrobial efficacy against most of the clinically relevant multidrug-resistant bacteria strains assessed (Garcia et al., 2022). It is the first study that reports on the phenolic composition of N. luridiformis and associates it with the mushroom’s antimicrobial activity. Water extracts were found to be more effective in terms of antimicrobial activity and were also found to contain higher concentrations for certain phenolic compounds compared to assessed methanol extract. The compounds 2,4-dihydroxybenzoic acid, homogentisic acid, and protocatechuic acid were the only three polyphenols common to both the aqueous and methanolic extracts. Protocatechuic acid was present in higher amounts in the aqueous extract, while higher levels of 2,4-dihydroxybenzoic acid were detected in the methanolic extract. In addition to the compounds mentioned above that were common to both extracts, methanol extracts contained additionally 4-Hydroxybenzoic acid and Vanillic acid. Importantly, none of the assessed extracts induced significant cytotoxicity in an MTT assay conducted with human foreskin fibroblast cells. In addition, the study by Garcia et al. first described the antibiofilm properties of N. luridiformis extracts (Garcia et al., 2022). In line with that, other studies also reported water extracts of wild mushrooms to be effective against bacterial and fungal pathogens (Gebreyohannes et al., 2013; Pinu et al., 2017).

Commercial mushroom species are better known in terms of composition; however, wild mushrooms are scarcely studied. Concerning the phenolic compounds profile, there are few studies with respect to the individual phenolics in wild edible mushrooms (Palacios et al., 2011). However, a study conducted by Alves et al. already back in 2013, concluded that phenolics are likely to be the active compounds responsible for the antimicrobial effect of wild mushrooms extracts (M. J. Alves et al., 2013) and they also identified 2,4-dihydroxybenzoic and protocatechuic acids as the main phenolic compounds with high activity against the majority of Gram-negative and Gram-positive bacteria (M. J. Alves et al., 2013).

The extracts of N. luridiformis assessed in the Garcia et al. study (Garcia et al., 2022) were also associated with antioxidant activity and observed effects of different solvents on the antioxidant activity of the extracts is worth noting. Aqueous extracts had markedly higher antioxidant capacities than the methanolic extracts, which let the authors to the conclusion that water is a more effective solvent for the extraction of antioxidant compounds from wild mushrooms than methanol. Moreover, the authors suggest that the difference in the antimicrobial activity of the assessed extract (aqueous and methanol) are due to the content of phenolic compounds, which was higher in aqueous extracts. In fact, several authors have previously associated the presence and content of phenolic compounds with the antimicrobial activity of different natural products (M. J. Alves & Pintado, o. J.; Barros et al., 2008; Bouarab-Chibane et al., 2019). In another study the therapeutic value of N. luridiformis was highlighted further (Alkan et al., 2020).  Amongst others, mushrooms extracts of N. luridiformis were found to have a significant anti-mutagenic potentials against several positive mutagens and in the same time does not exhibited mutagenic effects. Moreover, a potent antidiabetic activity of N. luridiformis extracts was demonstrated.

Health risk assessment

Atmospheric deposition of potentially toxic elements can contaminate forest ecosystems. Mushrooms subsequently can absorb these elements through their mycelium, even if the concentrations of elements in the substrate are low, and then transport them to the aboveground parts during fructification. The uptake and subsequent distribution of elements during fructification into the fruiting body are affected by several factors such as chemical composition of the substrate, location, species of mushroom, climatic conditions, age of the mycelium, number of fructification cycles, speed of fructification and age of the fruiting body. Due to a potential up-concentration of absorbed elements, mushrooms, especially from contaminated areas, may pose a risk to human health when consumed in excess. In this section maximum weekly intakes for the fresh weight of Neoboletus luridiformis are derived, that can be considered safe for long-term consumption. Since the studied species Neoboletus luridiformis is conditionally edible after 20 min of heat-treatment, the following risk assessment is considered applicable to mushrooms post-heat-treatment.

To derive the maximum safe intake of fresh Neoboletus luridiformis mushrooms per week, the acceptable weekly intake (AWI) for a specific element for an adult of 50 kg body weight is established in a first step. Therefore, literature was reviewed for latest study data to derive an up-to-date tolerable exposure level that is protective for a 50 kg adult for chronic exposure. If available, the calculation of the AWI value was based on the RfD values set by competent authorities. The concentration (C) of a specific element in Neoboletus luridiformis mushrooms has been established based on values detected in published biomonitoring studies. In Table 1 it is reported as the measured concentration of a specific element in the mushroom samples in µg/kg of fresh weight (FW). Intake stands for the consumption of the studied mushrooms (kg/week FW). If the consumed fresh weight of Neoboletus luridiformis mushrooms is greater than the estimated safe weekly consumption level (SWL), the consumption is considered potentially hazardous. If concentrations of elements were determined on a dry weight basis, the amount of the fresh weight was calculated based on the assumption that dry matter represents 10% in mushrooms (Kalač, 2010).

Some reviewed studies have assessed elements such as manganese (Mn), zinc (Zn), copper (Cu), cobalt (Co), and iron (Fe) that naturally occur in organisms and are required for catalytic activity of some enzymes at low concentrations. Typically, these elements occur in mushrooms in concentrations that are not of toxicological concern for humans. On the other hand, some elements such as lead (Pb), mercury (Hg), and cadmium (Cd) do not have a known role in metabolism and show toxic effects even when taken in low concentrations. Even though all the elements that have been assessed in a study are reported in the table below, the risk assessment is conducted only for typical environmental pollutants that may have toxic effects on humans in low concentrations.

Table 1: Studies assessing content of potentially toxic elements in Neoboletus luridiformis

Study details

Study results

(FW = fresh weight; DW = dry weight)

Potentially toxic element (PTE)

Max. Concentration (C)
adjusted to fresh weight basis* (µg/kg)

Acceptable weekly intake
(AWI) of toxic element** (µg)

Safe weekly consumption
level (SWL)**      
(AWI/C) [g/week FW]

Study site: Slovakia (38 locations) 

Year/Other: 2015–2019; 

Assessed elements: Hg 

Reference:
(Árvay et al., 2022)

Median mercury content:

> 5 mg/kg DW (4 locations characterized by
historical mining activities); 0.05 – 0.5 mg/kg DW (17 locations); 0.5 to 5.0
mg/kg DW (17 locations)

Hg

500

200

400

Study site: Belgrad Forest (Istanbul, Turkey) 

Year/Other: Oct 2020; 

Assessed elements: Cr, Se, P, Hg, Cu, Mn, Fe, Zn, Al, Ca, Mg, K

Reference: (Keskin et al., 2021)

Mean ± SD [mg/kg
DW]
:

Al: 49.2 ± 0.3; Ca: 15.4 ± 0.3; Cu: 37.56 ± 0.12;
Cr: 0.15 ± 0.08; Fe: 61.2 ± 0.7; Hg: 15.27 ± 0.58; K: 12665 ± 45; Mg: 618 ± 3; Mn: 8.31 ± 0.04; P: 5.23 ± 0.02; Se: 1.38 ± 0.14; Zn: 88.7 ± 0.6

Cu

3,768

35,000

9,288

Cr

23

550

23,913

Hg

1,585

200

126

Zn

8,930

37,500

4,199

Study site: Bohemian Forest, the Czech Republic; 

Year/Other: Sep 2020 – Oct 2022; 

Assessed elements: Ag, Al, As, Be, Ca, Cd, Co, Cr, Cu, Fe, Li, Mg, Mn, Ni, Pb, Rb, Se, Tl, Zn

Reference: (Krejsa et al., 2024)

Mean ± SD, (min-max) [mg/kg DW]

Ag: 4.0 ± 2.7, (1.0–9.7); Al: 20 ± 15, (6–55); As: 5.1 ± 1.7, (2.2–7.5); Be: 0.013 ± 0.011, (0.005–0.037); Ca: 97 ± 39, (60–210); Cd: 0.67 ± 0.65, (0.10–2.3); Co: 0.11 ± 0.08, (0.02–0.25);
Cr: 0.21 ± 0.12, (0.08–0.52); Cu: 37 ± 14, (15–60); Fe:
79 ± 30, (46–140); Li: 0.38 ± 0.13, (0.24–0.58); Mg: 910 ± 180 (610–1200); Mn: 7.2 ± 2.8, (3.8–13); Ni: 0.83 ± 0.45, (0.28-1.8); Pb: <0.01–0.35; Rb: 590± 270, (320–1200); Se: 2.2 ± 0.7, (0.4–3.3); Tl: <0.10–0.20; Zn: 160 ± 60, (70–310)

As

750

750

1,000

Cd

230

125

543

Cr

52

550

10,576

Cu

6,000

35,000

5,833

Rb

120,000

155,000

1,291

Zn

31,000

37,500

1,210

Study site: Jeseníky Mountains, Czech Republic; Year/Other: NA; 

Assessed elements: Cd, Cu, Pb, Zn; 

Reference: (Pecina et al., 2022)

Mean ± SD [mg/kg
DW]
:

Cd: 3.04 ± 2.53; Cu: 29.4 ± 8.51; Pb: 0.90 ± 0.73;
Zn: 302 ± 84.1

Cd

557

125

224

Cu

3,791

35,000

9,232

Pb

163

150

920

Zn

38,610

37,500

971

*The dry weight (DW) content of both wild and cultivated mushrooms is quite low, typically ranging between 80 and 140 grams per kilogram. For fresh weight (FW) adjustments, a standard value of 100 grams per kilogram is used for calculations (DW = FW/10); **Derived for an adult of 50kg body weight. 

Studies assessing content of potentially toxic elements in Neoboletus luridiformis

The reviewed studies (see Table 1) have expressed the contents of elements (mg/kg DM) determined for N. luridiformis in parameters such as average, standard deviation (SD), median, and range (minimum–maximum) values. In the original study papers, all values were reported on a dry weight basis. For the estimation of the maximum concentration found in a study and adjustment to fresh weight basis, the maximum of the range was taken if reported, otherwise the mean+1xSD was used. An exception to this is the study published by Arvey et al. (Árvay et al., 2022). As this study reported only median values, the median was used for the estimation of the maximum concentration (C) on fresh weight basis. Moreover, in this study samples picked from sites with reported historic mining activity were not considered, as these are not considered representative for the average wild mushroom collected.

In the study conducted by Krejsa et al., N. luridiformis was found to accumulated Rb, Ag, Se, Cd, Cu, and Zn with average bioconcentration factors (BCF) of 15, 8.6, 7.4, 3.0, 2.0, and 1.6, respectively (Krejsa et al., 2024). Similarly, in the study conducted by Pecina et al. that assessed only the elements Cd, Cu, Pb and Zn, the elements Cd, Cu, and Zn were identified as strong accumulators from the soil (Pecina et al., 2022). The study found bioconcentration factors (BCF) of up to 6,920, 5.45, and 10.1 for Cd, Cu, and Zn, respectively. BCF values > 1 are common for mushrooms, and often values in the order of tens to hundreds are reached. However, the general absence of stronger relationships between the soil and mushroom elemental contents and the extreme values observed for Cd (BCF > 1000) led the authors of the Pecina et al. study to speculate that another accumulation mechanism than the uptake from bulk soil was of importance.

Mercury (Hg):

The mercury content in mushrooms is almost entirely inorganic mercury and the amounts of methyl mercury found are practically negligible, becoming, in the worst case, less than 13% of total mercury (Asensio, 2023). Based on this, the provisional tolerable weekly intake of 0.004 mg/kg body weight derived for mercury by JECFA, leads to a safe acceptable weekly intake (AWI) of 200 µg for an adult of 50kg body weight.

The study conducted by Arvey et al. at various study sites in Slovakia found that the content of mercury in the fruiting bodies of N. luridiformis correlates directly with the mercury content in the soil/substrate of the respective study site (Árvay et al., 2022). The highest mercury content in fruiting bodies were found in four localities that were all characterized by their historical mining and metalworking activities. In these localities the median mercury content was above 5 mg/kg dry weight. In other study sites the median mercury content ranged from 0.05 to 0.5 mg/kg dry weight (17 localities) and from 0.5 to 5.0 mg/kg dry weight (17 localities). From the entire set of mushroom samples (n = 2 × 378), 216 cap samples had concentrations less than 1 mg/kg, 61 cap samples had concentrations between 1 and 5 mg/kg, 28 cap samples had concentrations greater than 5 mg/kg, 256 stipe samples had concentrations less than 1 mg/kg, 36 stipe samples had concentrations between 1 and 5 mg/kg, and 9 stipe samples had concentrations greater than 5 mg/kg.

Cadmium (Cd):

Food is the major source of cadmium exposure for the non-smoking general population. Cadmium exerts toxic effects after long-term exposure mostly on the kidney but also on the bones. In 2011 the EFSA Panel on Contaminants in the Food Chain (CONTAM) reexamined available toxicity data for cadmium and concluded that the tolerable weekly intake (TWI) for cadmium established in 2009 of 2.5 μg/kg bodyweight should be maintained in order to ensure a high level of protection of consumers, including subgroups of the population such as children, vegetarians or people living in highly contaminated areas (EFSA, 2009, 2011). This leads to a safe acceptable weekly intake (AWI) of 125 µg for an adult of 50kg body weight.

Cupper (Cu):

Copper is an essential micronutrient and also a regulated product used in organic and in conventional farming pest management. Both deficiency and excessive exposure to copper can have adverse health effects. Based on an updated evaluation of the scientific evidence, EFSA hast recently update the acceptable daily intake (ADI) for copper from all sources in food. The ADI has been reduced from 0.15 mg/kg of body weight (bw) to 0.07 mg/kg bw (More et al., o. J.). This translates into a safe acceptable weekly intake (AWI) of 35,000 µg for an adult of 50kg body weight.

Chromium (Cr):

While chromium exhibits several oxidation states, the two most stable forms are trivalent chromium [Cr(III)] and hexavalent chromium [Cr(VI)]. Trivalent chromium is significantly less toxic than hexavalent chromium because it enters cells less readily and is less likely to cause damage. Ingested hexavalent chromium can be reduced to the less toxic trivalent form in the gastrointestinal tract. However, some of the ingested hexavalent chromium can bypass this process and enter cells, to cause potential DNA damage that may lead to cancer and other adverse health effects. As hexavalent chromium is the more toxic of the two stable chromium forms, it is used to derive an acceptable intake level.

In 1998 based on a study of rats ingesting K2CrO4 in water for one year an oral reference dose of 3 μg/kg/day was set by the EPA. In the toxicological profile for chromium established by the ATSDR, a minimal risk level (MRL) of 5 μg/kg/day has been derived for intermediate-duration oral exposure to hexavalent chromium compounds. for hematological effects in rats based on data from a study by NTP. More recently, in 2018, Health Canada derived a reference value of 2.2 μg/kg/day (Health Canada, 2016). This was based on a 90-day sodium dichromate dihydrate water study in B6C3F1 mice (Thompson et al., 2011). Using the most recent and critical reference value derived by Health Canada, this translates into a safe acceptable weekly intake (AWI) of 550 µg for an adult of 50kg body weight.

Arsenic (As):

Arsenic occurs naturally in the environment but industrial emissions and its use in fertilizers and pesticides have contributed to increased levels. Food and drinking water are the main sources of exposure to arsenic. In 2010 the Joint FAO/WHO Expert Committee on Food Additives (JECFA) withdrew its provisional tolerable weekly intake of arsenic (15 μg/kg body weight) after adverse effects were reported at lower levels of exposure (EFSA, 2024). As a result, a new EU regulation (2023/465) was established to set maximum levels of arsenic in certain foods. The lowest limit set for food intended for adults was set for non-parboiled milled rice with 0.15 (mg/kg wet weight). Assuming that the average adult eats 2 kg food on average, leads to an acceptable intake of 300 μg of Arsenic per day and 1500 μg of Arsenic per week.

In 2009, the EFSA CONTAM Panel assessed the risks to human health related to the presence of arsenic in food. The Panel noted that the main adverse effects reported to be associated with long-term ingestion of inorganic Arsenic in humans are skin lesions, cancer, developmental toxicity, neurotoxicity, cardiovascular diseases, abnormal glucose metabolism and diabetes. A provisional tolerable weekly intake (PTWI) of 15 μg/kg bw was established by the Joint FAO/WHO Expert Committee on Food Additives (JECFA) in 1983. Since then, data have shown that oral exposure to inorganic Arsenic causes cancers of the lung and urinary bladder in addition to skin, and a range of other adverse effects had also been reported at exposures lower than in the studies reviewed by JECFA. Therefore, the CONTAM Panel concluded that the JECFA PTWI was no longer appropriate. The CONTAM Panel identified cancers of the urinary bladder, lung and skin, and skin lesions, as the most relevant endpoints for providing an appropriate Reference Point to be used in the risk characterization. Extrapolating the established PTWI by JEFCA to an average adult of 50 kg, leads to an acceptable intake of 750 μg of Arsenic per week. As this is lower than the value derived based on the limits for Arsenic specified in the new EU regulation (2023/465), the 750 μg/week is applied as the acceptable weekly intake (AWI) in the risk assessment on hand.

Rubidium (Rb):

Rubidium, like sodium and potassium, almost always has +1 oxidation state when dissolved in water, even in biological contexts. The human body tends to treat Rb+ ions as if they were potassium ions, and therefore concentrates rubidium in the body’s intracellular fluid (i.e., inside cells) (Relman, 1956). The ions are not particularly toxic; a 70 kg person contains on average 0.36 g of rubidium, and an increase in this value by 50 to 100 times did not show negative effects in test persons. The biological half-life of rubidium in humans measures 31–46 days. Although a partial substitution of potassium by rubidium is possible, when more than 50% of the potassium in the muscle tissue of rats was replaced with rubidium, the rats died. Assuming that the weekly dietary consumption of half of the amount an average person contains (0.155 g of rubidium) has no adverse effects, gives a safe acceptable weekly intake (AWI) of 155,000 µg for an adult.

Lead (Pb):

Lead (Pb) is accumulated in the body in a variety of tissues and organs and can give many different toxic effects in large enough doses. The main effects of long-term exposure to low doses of lead are on the nervous system. Small children, and foetuses in particular, are most vulnerable, and exposure to lead could result in reduced cognitive and motoric development. These effects of lead are well documented and have also been confirmed through epidemiological studies. Based on the effects on children and foetuses, the PTWI for lead was set to 25 µg/kg body weight in 1986 by the Joint FAO/WHO Expert Committee on Food Additives (JECFA). In 1993 and 2000, JECFA confirmed this PTWI value and extended it to apply to all ages. In 2004, the European Food Safety Authority (EFSA)’s Scientific Panel on Contaminants in the Food Chain has issued a revised opinion in which they conclude that lead contamination of food is regarded as a public health problem because new data could indicate that mental and cognitive development in foetuses and small children might be inhibited even by quantities of lead previously thought to be safe.

The Committee considered the neurodevelopmental effects of lead to be pivotal in its assessment for children. Based on the results of a meta-analysis of epidemiological data, the chronic dietary exposure corresponding to a decrease of 1 IQ point was estimated to be 0.6 μg/kg bw/d (5th to 95th: percentiles 0.2–7.2 μg/kg bw/d). For adults, the Committee concluded that the pivotal data were the increased systolic blood pressures. Based on the averaged median reference slope estimates for blood lead levels versus systolic blood pressure from four epidemiology studies, the dietary exposure corresponding to an increase in systolic blood pressure of 1 mmHg (0.1333 kPa) was estimated to be 1.3 (5th to 95th percentiles 0.6–28) μg/kg bw/d. Based on this analysis, the previously established PTWI of 25 mcg/kg bw is associated with a decrease of at least 3 IQ points in children and an increase in systolic blood pressure of approximately 3 mmHg (0.4 kPa) in adults. These changes are important when viewed as a shift in the distribution of IQ or blood pressure within a population. The Committee concluded that the PTWI could no longer be considered health protective, and it was withdrawn. Taking the 5th percentile for the increase in systolic blood pressure in adults (0.6 μg/kg bw/d) a safe acceptable weekly intake (AWI) of 150 µg can be established for an adult of 50 kg.

Zinc (Zn):

The D-A-CH Societies derived recommendations for dietary intake of zinc that are at 11.0 mg/day and 14.0 mg/day for females and males, respectively, between 15 and 18 years of age. For adults, the recommended intake values range between 7 and 16 mg per day, depending on phytate intake. The European Food Safety Authority (EFSA) derived Population Reference Intake values for zinc of 11.9 mg (female) and 14.2 mg/day (male) for adolescents aged 15 to 17 years. For adults, intake recommendations between 7.5 and 16.3 mg/day were derived depending on the daily phytate intake (EFSA, 2014). Taking the lower limit of this range, this translates into a safe acceptable weekly intake (AWI) of 37,500 µg for an adult.

Discussion

Neoboletus luridiformis mushrooms are regularly consumed where they occur and have been associated with various potential health benefits, including antimicrobial, antioxidative, and antimutagenic activity. However, due to a potential up-concentration of potentially toxic elements, mushrooms, especially from contaminated areas, may pose a risk to human health when consumed in excess. Sold mushrooms are rarely tested for their actual contamination with potentially detrimental elements and the weight of mushrooms that could be eaten safely often remains unclear to consumers. The aim of this review was to get an overview of the chemical composition, nutritional value and potential health benefits of Neoboletus luridiformis and derive dietary recommendations which would keep negative health impacts from potentially detrimental elements in fruiting bodies on an acceptable level.

From the elements examined in the various studies listed in Table 1, mercury (Hg) has been identified as the element limiting the safe weekly consumption level (SWL) of N. luridiformis mushrooms the most. With the highest mercury concentration of 1,585 µg/kg found in the study from Keskin et al. only 126 g of fresh N. luridiformis mushrooms per week can be considered safe for dietary consumption (Keskin et al., 2021). In terms of limiting the safe weekly consumption level, mercury is followed by cadmium (Cd), which allows for a maximum safe weekly consumption of 224 g when occurring in the concentrations observed in the Pecina et al. study (Pecina et al., 2022). Least restricting in terms safe weekly consumption are the observed contents of chrome (Cr) followed by the contents of cupper (Cu).

Knowing the characteristics of the site a mushroom originates from, allows to reduce the likelihood of exceptional high mercury concentrations and therefore the potential for negative health impacts. Mercury in the fruiting bodies of N. luridiformis were found to correlate directly with the mercury content in the soil/substrate of the site they originate from (Árvay et al., 2022). Other environmental factors, associated with the uptake and distribution of potentially toxic elements into the fruiting bodies of mushrooms are factors such as chemical composition of the substrate, location, climatic conditions, age of the mycelium, number of fructification cycles, speed of fructification and age of the fruiting body. N. luridiformis mushrooms, from contaminated areas such as historic mining sites should therefore be prevented in dietary, whereas N. luridiformis mushrooms from remote sites not affected by historic mining activities can generally be considered of higher quality in terms of contamination with potentially toxic elements.

Hence, if a high anthropogenic contamination of the site a N. luridiformis mushroom originates from can be excluded up to 400 g of fresh N. luridiformis mushrooms per week can be considered safe for dietary consumption for the average adult. In contrast, if a high anthropogenic contamination is likely, the weekly dietary consumption should be restricted to 200 g the most. Susceptible subgroups like pregnant woman and women of childbearing age should avoid the consumption of N. luridiformis mushrooms completely due to their potential mercury content, or the most consume only half of the intake derived for the average adult.

In summary, N. luridiformis mushrooms can be considered a valuable dietary supplement due to their various health benefits when health risks arising from the content of potentially detrimental element is kept low, by restricting the weekly consumption appropriately.