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Study of Biological Activity of Tricholoma Equestre Fruiting Bodies and Their Safety for Human

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Study of Biological Activity of Tricholoma Equestre Fruiting Bodies and Their Safety for Human View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Jagiellonian Univeristy Repository European Food Research and Technology (2018) 244:2255–2264 https://doi.org/10.1007/s00217-018-3134-0 ORIGINAL PAPER Study of biological activity of Tricholoma equestre fruiting bodies and their safety for human Bożena Muszyńska1 · Katarzyna Kała1 · Jelena Radović2 · Katarzyna Sułkowska‑Ziaja1 · Agata Krakowska3 · Joanna Gdula‑Argasińska4 · Włodzimierz Opoka3 · Tatjana Kundaković2 Received: 11 June 2018 / Revised: 3 July 2018 / Accepted: 6 July 2018 / Published online: 31 July 2018 © The Author(s) 2018 Abstract One of the species of mushrooms authorized for sale in some countries—Tricholoma equestre—can be harmful, and its excessive consumption can lead to serious health problems. Many authors have pointed to the relationship between the consumption of the T. equestre and the occurrence of rhabdomyolysis. The aim of this study was to analyze the composition of biologically active substances in the T. equestre fruiting bodies, and determine their biological activity. The main aim of the analyses performed in the present study was to determine whether the T. equestre is safe or dangerous for consumption by humans. The obtained results, in addition to the existing reports on poisoning caused by T. equestre consumption, are another reason to not take the risk of consuming the fruiting bodies of this species, as the natural environment is rich in other species of edible mushrooms that are not only tasty, but also exhibit healing properties. Keywords Antioxidant activity · Pro-inflammatory activity · Edible mushrooms · Tricholoma equestre · Rhabdomyolysis Introduction flavovirens)—can be harmful, and its excessive consumption can lead to health problems [1–7]. Edible mushrooms have been valued for years because Many authors have pointed to the relationship between of their dietary qualities and healing properties. In recent the consumption of the T. equestre fruiting bodies and the years, the list of edible and medicinal mushrooms has been occurrence of rhabdomyolysis, i.e., rapid decomposition of expanded [1]. In Poland, 44 species of edible and medicinal transverse striated muscle tissue [1, 4–7]. Rhabdomyolysis mushrooms were identified. They were included in the offi- is a clinical condition, whose very frequent consequence is cial list of “fungi authorized for the market or production death. The characteristic symptoms include general weak- of mushroom products and foods containing mushrooms,” ness, muscle pain, sweating without symptoms of fever, which is an annexure to the Ordinance of the Minister of and dark urine color [1, 4, 5]. No other possible causes of Health of 17 May 2011. However, some scholars have rhabdomyolysis (viral, parasitic, immunological diseases, reported that one of the widely admitted species on the previous injuries, or adverse drug reactions) were found list—Tricholoma equestre (also referred to as Tricholoma in patients, whose cases were analyzed after they had con- sumed large amounts of the T. equestre fruiting bodies [1, 4–7]. * Bożena Muszyńska [email protected] In several European countries, e.g., in France or Germany, the T. equestre species is considered dangerous because of 1 Department of Pharmaceutical Botany, Faculty of Pharmacy, the fact that in the years 1992–2016, there were numerous Jagiellonian University Medical College, Kraków, Poland cases of poisoning as a result of its consumption, including 2 Department of Pharmacognosy, Faculty of Pharmacy, several deaths. Some cases of the above-mentioned fatal poi- University of Belgrade, Belgrade, Serbia soning were also reported in Poland [1, 4, 5, 7]. Fatal cases 3 Department of Inorganic and Analytical Chemistry, Faculty were reported as a result of the repeated consumption of of Pharmacy, Jagiellonian University Medical College, significant amounts of this species of fruiting bodies as part Kraków, Poland of several subsequent meals [4–6, 8]. Here, repeated con- 4 Department of Radioligands, Faculty of Pharmacy, sumption is defined as a triple meal consisting of 100–400 g Jagiellonian University Medical College, Kraków, Poland Vol.:(0123456789)1 3 2256 European Food Research and Technology (2018) 244:2255–2264 of appropriately prepared fresh fruiting bodies [7, 8]. The presence of sterols, and determine the antioxidant, antibac- first 12 cases of poisoning after the consumption of the T. terial, antifungal, and anti-inflammatory activity. The main equestre fruit bodies were found in France in 1992–2001 aim of the analyses performed in the present study was to [2, 4, 7–9]. determine whether the T. equestre fruiting bodies are safe After these events, experiments were carried out involv- or dangerous for consumption by humans. ing the administration of a T. equestre extract to laboratory animals (mice), which confirmed its toxic activity, manifest- ing in the increase in the blood levels of the biochemical markers of toxicity: plasmatic creatine kinase (CK), bili- Materials and methods rubin, alanine aminotransferase (ALAT), or aspartate ami- notransferase (AST). In addition, the animals had diarrhea, Mushroom materials showed reduced motor activity, and had disintegrated muscle fibers. Unfortunately, it was not possible to identify a spe- In the present work, the fruiting bodies of T. equestre (L.) cific myolytic toxin, which was responsible for rhabdomy- P. Kumm. (Tricholomataceae) also known as T. flavovirens olysis; this also made it impossible to investigate the mecha- were used. These fruiting bodies were collected from the nism of this toxin action. It turned out that this species, in mixed forests of South Poland (in the vicinity of Kraków addition to its myolytic activity, exhibits a strong cardio- and and Rzeszów) between 2014 and 2016. The taxonomic hepatotoxic effect, which contributes to the impression of identification of the sporocarps was performed using the rhabdomyolysis [1, 4, 5, 7, 8]. Studies conducted on mice method proposed by Knudsen and Vesterholt and the key confirmed the toxicity, but they did not definitively confirm (http://www.mycokey.com ) developed by Muszyńska [13]. that the consumption of T. equestre was the cause of the fatal Representative voucher specimens number KB/Tr2016 poisoning; nevertheless, the authors warned against collect- were deposited at the Jagiellonian University Collegium ing, buying, and above all, repeatedly consuming the fruiting Medicum (Kraków, Poland) in the Department of Phar- bodies of this species [5, 8]. maceutical Botany. The mushroom materials were frozen On the basis of mycorrhiza, two varieties of fruiting and then lyophilized (Freezone 4.5. Labconco; − 40 °C) to bodies are distinguished within the T. equestre species: one obtain the mushroom samples for further analyses. showing symbiosis with Populus sp., and the other with Betula sp. This may be the reason for the differences in the content of biologically active substances. In Poland, this spe- Reagents cies is considered edible, while in France, its distribution and consumption has been banned since 2005 [5]. Certainly, Cyclohexane and dichloromethane were purchased from there have been many reports on the positive effects of the Thermo Fisher Scientific, Life Technologies (Waltham, consumption of T. equestre on human health. The antican- MA, USA); methanol, 1,1-diphenyl-2-picrylhydrazyl, and cer activity was demonstrated for flavomannin-6,6′-dimethyl FAME were obtained from Sigma (St. Louis, MO, USA). ether isolated from the fruiting bodies of this species. It was Ascorbic acid was purchased from Acros (Geel, Belgium); demonstrated that even temperature-treated fungi are a good rutin from Fluka (Buchs, Switzerland); gallic acid from source of this compound and have a positive antiproliferative Roth (Karlsruhe, Germany); petrolether from Centrohem effect on the CaCo-2 colorectal cancer cells [10]. T. equestre (Stara Pazova, Serbia); pepsin and bile salts from BTL is also a source of zinc—an element that is necessary for (Łódź, Poland); MgCl2 from Chempur (Kraków, Poland); the appropriate functioning of the human body [11]. It is a NaHCO3 from PPH Golpharm (Kraków, Poland); KOH species in which unsaturated fatty acids were determined. and NaCl from Alfa Aesar® (Kandel, Germany); CaCl2 Therefore, the prevention of cardiovascular diseases (e.g., from Pharma Zentrale GmbH (Herdecke, Germany); HCl ® hypertension and atherosclerosis) is indirectly attributed pancreatic extract, HNO3 concentrated, Suprapur , and to this species. Among the fatty acids, T. equestre contains hydrogen peroxide 30% from Merck (Darmstad, Ger- oleic acid (a popular component of olive oil) in the larg- many); KHCO3, Na2HPO4, C6H8O7, and K2HPO4 from est amounts, whose most important activity is to counteract Polish Company of Chemistry (Gliwice, Poland); and zinc hypercholesterolemia. Moreover, the presence of linoleic (II) ion content standards at a concentration of 1 g/L from acid, which is biologically significant for the body, was Regional Office of Measures (Łódź, Poland). Quadruple- determined in this species [12]. distilled water with a conductivity of less than 1 µS/cm The aim of this study was to analyze the composition was obtained using an S2–97A2 distillation apparatus of biologically active substances in the T. equestre spe- (Chemland, Stargard Szczeciński, Poland). cies, including bioelements (in vitro conditions imitating natural digestive processes), profile fatty acids, identify the 1 3 European Food Research
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