Article
Edible mushroom-related poisoning: A study on circumstances of mushroom collection, transport, and storage
Human and Experimental Toxicology 1–7 ª The Author(s) 2014 Reprints and permission: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0960327114557901 het.sagepub.com
T Gawlikowski1, M Romek2 and L Satora3
Abstract Background: The American Association of Poison Control Center (AAPCC) shows that in 2012 there were 0.3% of human exposures involving mushrooms. Only 17% of 6600 cases were then identified by the species. The present retrospective study was designed to identify the epidemiology of mushroom poisoning in adults admitted to Krakow’s Department of Clinical Toxicology (DCT) from 2002 to 2009. Materials and Methods: This study was conducted retrospectively after examining the files of 457 adult patients with wild mushroom poisoning. Mycological analysis was made and the species of the poisoninginducing mushroom was determined. Furthermore, the circumstances related to the mushroom gathering, transport, storage, preparation, and consumption have been analyzed. Results: The analysis revealed that in 400 (87.53%) out of 457 cases, the clinical symptoms were caused by ingestion of identified edible mushroom species. The main reason for edible mushroom poisoning is associated with their incorrect processing after harvest. The analysis of the circumstances of mushroom collection, transport, and storage shows that the largest percentage of poisoning was connected with long-term storage of mushroom dishes, collecting, and storing them in plastic bags, and long storage of mushrooms. Conclusion: Based on spore analysis of the gastric content, edible mushrooms were responsible for the great majority of mushroom poisoning cases admitted to the DCT. The toxicity of edible mushroom is associated with proceeding with them during collection, transport, and storage. The medical history should be supplemented by questions concerning these circumstances. The identification of the mushroom by a mycologist is highly desirable. Keywords Edible mushroom poisoning, epidemiology, mycologist
Introduction The gathering and consumption of wild mushrooms is a traditional social outing in Europe, Asia, and the United States. 1–5 Mushrooms were described also as popular remedies in ancient oriental documents, and some of them became ingredients in traditional medicine.6 The consumption of wild mushrooms is very popular in Poland. An estimated figure of over 10 million Poles participate in mushroom hunts each year, and from 18,000 to 20,000 tons of wild mushrooms are harvested annually, usually for personal consumption. From about 10,000 species of mushroom about 50–100 species are poisonous.7 It is important to note that the most mushroomderived toxins poisonous to humans are resistant to
cooking, canning, freezing, or any other processing method. Therefore, the only way to avoid poisoning is to avoid consumption of the toxic species. There are
1
Department of Clinical Toxicology, Jagiellonian University Medical College, Krakow, Poland 2 Department of Cytology and Histology, Institute of Zoology Jagiellonian University, Krakow, Poland 3 Department of Physiology and Reproduction of Animals, University of Rzeszow, Rzeszow, Poland Corresponding author: T Gawlikowski, Department of Clinical Toxicology, Jagiellonian University Medical College, ul. Sniadeckich 10, Krakow, 31501, Poland. Email: [email protected]
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no universal clinical care guidelines for the cases of mushroom poisoning. The choice of treatment is guided by the clinical symptoms, and for most mushroom toxins there is no antidote.8 Modern methods of intensive care medicine have reduced mushroom mortality and morbidity substantially.1,4 The diagnosis of mushroom poisoning should be based on mushroom identification, clinical features, and laboratory analyses.9 Mushrooms have numerous spores characteristic for each species.10,11 The gastric contents, the reminder of a mushroom dish, and the whole mushrooms themselves are subject to evaluation. Most literature related to mushroom exposures and poisonings are clinical case reports, with few studies characterizing the epidemiology of exposures.12 Additionally, in medical literature, there are studies investigating exposure to toxic mushrooms and subsequent hospitalizations in the United States3,12,13 but comparable studies in Europe appear seldom, to our knowledge.2,9 The observations supported by data in the literature indicated edible species as the most common cause of mushroom poisoning.2,11 Since edible mushrooms do not have specific toxins, what is the cause of their toxicity? The preliminary study led us to believe that the circumstances of mushroom collection, transport, and storage might be related to the edible mushroom poisonings.14 The study group consists of wild mushroom-poisoned adult patients admitted to the Department of Clinical Toxicology (DCT), Jagiellonian University Medical College in Krakow, Poland. In each case of mushroom poisoning, the detailed interview concerning the proceeding with mushroom during and after collection, and the mushroom dish was done.14 The specialist mycologist made a spore analysis of the gastric contents and identified mushroom species. We performed this study to present descriptive epidemiological data on mushroom enquiries to the DCT in Krakow, with particular attention to the circumstances of their collection, transportation, and storage. The results have been compared with literature data.11
Materials and methods This study was conducted retrospectively after examining the files of adult (18 years and older) patients with wild mushroom poisoning who were admitted to the DCT from 2002 to 2009. The referral population, in Southeast Poland, amounts to about 7 million
people. Demographic and detailed clinical information on exposure cases, circumstances of poisoning, symptoms, and the causality are recorded in a systematic and standardized manner by a physician trained in clinical toxicology. On admission to the DCT, the form concerning the circumstances related to the mushroom gathering, transport, storage, preparation, and consumption was completed.14 A detailed history was taken from each patient. The database was reviewed by one doctor specializing in clinical toxicology. The diagnosis of mushroom poisoning was based on the history provided by the patients, symptoms, and physical examination. The laboratory tests conducted included blood analysis namely electrolytes (sodium and potassium), creatinine, glucose, alanine aminotransferase, aspartate aminotransferase, creatine kinase, total bilirubin, blood cell counts (red blood cells, white blood cells, hematocrit, hemoglobin, and platelets), and prothrombin time expressed as the international normalized ratio index. Additionally, when Amanita phalloides poisoning was suspected, urine analysis used for amanitin was conducted. Patients with co-ingestion of drugs in overdose or drugs of abuse, affected by diseases of the digestive system, and subjects treated with medicine that might affect gastrointestinal function were not enrolled. Febrile patients were excluded from the study because of infection suspicion, which could be responsible for reported complaints. In all of the included cases, the specialist mycologist made a spore analysis of the gastric contents. Microscopic examination of the gastric contents is aimed at determining the presence of spores and spore identification. The species of the poison-inducing mushroom was determined in all included cases. Spore analysis was made with the use of a light microscope (type Olympus BX 50-F, Japan). Two microscopic specimens were made, one stained with Lugol’s solution, while the other one was not stained. The spores were evaluated at a magnification of 400. The spores that were found were identified using atlases and then compared with the model spores—specimens of spores of a specific mushroom species. The spore models were obtained from mushrooms collected and identified by a specialist mycologist. The dried model sporocarps of mushrooms, containing spores, were stored in sealed containers. The preparation of the model spores was conducted at the same time as the mycological analysis of spores obtained from a poisoned patient. All the preparations were stained in the same way.
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Figure 1. Monthly variation for cases of mushroom poisoning reported to the Department of Clinical Toxicology in the years 2002–2009.
The results were compared with data that referred the mushroom species responsible for poisoning from the Regional Centre of Acute Poisoning in Sosnowiec (RCAPS), Southwest Poland, with 10 million population.11 The same methods of spore analysis were used by RCAPS. The statistical analysis was performed using the STATISTICA data analysis software system, version 10 (StatSoft. Inc. 2011). We calculated the percentage p of poisoning caused by different edible and toxic species as well as the percentage of poisoning caused by the mushroom collection method and the percentage of poisoning under different circumstances concerning the collection of the mushrooms, their transport, and their storage as a ratio for the total number of poisoned people by edible species only. The differences between the analyzed groups were detected using a Fisher–Snedecor test. The present retrospective study was designed to identify the epidemiology of mushroom poisoning in adults from 2002 to 2009. Furthermore, the circumstances of mushroom collection, transport, and storage have been analyzed.
Results We identified 457 patients poisoned by wild mushrooms (mean age 43.81 + 18.53 years; 62.8% female) during the study period, among a total of 18,043 poisoning cases, where the frequency of wild mushroom poisoning was 2.53%. Apart from
mushrooms that contain psychoactive toxins, the ingestion of toxic mushrooms was accidental and caused by misidentification of species. August, September, and October were the peak months for mushroom poisoning (Figure 1), and these months are generally warm and rainy. In 400 ( p ¼ 87.53%) out of 457 cases, the mycological analysis revealed that the clinical symptoms were caused by ingestion of identified edible mushroom species (Table 1). The symptoms of patients with edible mushroom poisoning were vomiting ( p ¼ 82%), nausea ( p ¼ 68%), abdominal discomfort ( p ¼ 58%), and diarrhoea ( p ¼ 38%), and they occurred within 30 min to 4 h of the intake of a dish containing the mushrooms and subsided after 1–3 days. During that time, laboratory tests did not reveal any significant abnormalities. In all of the cases, gastric lavage and a single dose of charcoal were administrated (1 g kg1 body weight). On the first day of the treatment, a light diet was initiated, and the water and electrolyte imbalance was compensated intravenously, if necessary. Only isotonic fluids were used for intravenous infusions. Saline was preferred. When the gastrointestinal symptoms subsided, the diet limitations were lifted. No laxatives, antiemetics, or antidiarrhoeal medication were administered. The duration of the treatment was 1–3 days. In 21 cases (5.25%), the patients were hospitalized when pernicious vomiting and colliquative diarrhoea occurred. The edible mushroom species identified as the most
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Table 1. Poisoning caused by different species of mushrooms (edible and toxic) observed by the DCT in the years 2002–2009. Mushroom
N
p [%]
Edible species Armillariella mellea (Vahl) P. Kumm.1871 53 11.60 Physalacriaceae Macrolepiota procera (Scop.) Singer 1948 39 8.53 Agaricaceae Suillus luteus (L.) Roussel 1796 Suillaceae 37 8.10 Cantharellus cibarius Fr. 1821 Cantharellaceae 36 7.88 Agaricus campestris L. 1753 Agaricaceae 35 7.66 Xerocomus (Boletus) badius (Fr.) Fr. 1832 28 6.13 Boletaceae Russula virescens (Schaeff.) Fr. 1836 28 6.13 Russulaceae Boletus edulis Bull. 1782 Boletaceae 22 4.81 Lactarius deliciousus (L.) Gray 1821 Russulaceae 22 4.81 Leccinum aurantiacum (Bull.) Gray 1821 21 4.59 Boletaceae Tricholoma equestre (L.) P. Kumm. 1871 21 4.59 Tricholomataceae Clitocybe gibba (Pers.) P. Kumm. 1871 20 4.38 Tricholomataceae Marasmius oreades (Bolton) Fr. 1836 19 4.16 Marasmiaceae Leccinum scabrum (Bull.) Gray 1821 Boletaceae 19 4.16 Sum 400 87.53 Toxic species Amanita phalloides group 40 8.75 Hallucinogenic mushrooms 12 2.62 Boletus satanas Lenz 1831 Boletaceae 2 0.44 Hypholoma fasciculare (Huds.) P. Kumm 1871 2 0.44 Strophariaceae Entoloma sinuatum (Bull.) P. Kumm.1871 1 0.22 Entolomataceae Sum 57 12.47 DCT: Department of Clinical Toxicology in Krakow. N: number of poisoning; p: percentages of poisoning [%] of the total poisoning caused by both, edible and toxic species; n ¼ 457 total cases of poisoning.
common causes for poisoning were the honey mushroom Armillariella mellea, the parasol mushroom Macrolepiota procera, the sticky bum Suillus luteus, the chanterelle Cantharellus cibarius, the field mushroom Agaricus campestris, the Bay Bolete Boletus badius, and the green-cracking Russula Russula virescens (Table 1). The results of the mycological analysis are reported in Table 1. These analyses were carried out among patients of DCT in the years 2002–2009. It was shown that the incidences of poisonings were caused by both edible and toxic species of mushrooms. Statistically significant differences existed between the percentages
Table 2. The mushroom gaining method used by poisoned patients of the DCT in the years 2002–2009. Methods of mushroom gaining Independent mushroom collection Purchase from a person near road Purchase at market Purchase in a shop
N
p [%]
284 54 44 18
71.00 13.50 11.00 4.50
DCT: Department of Clinical Toxicology in Krakow. N: number of poisoning; p: percentage of the mushrooms gaining methods used by poisoned patients by edible species only [%]; n ¼ 400 of the total poisoning cases caused by edible species.
of poisoning caused by different mushroom species (value of the Fisher–Snedecor statistics F ¼ 8.74, critical value of the Fisher–Snedecor statistics Fa12 ¼ 1.614, where a ¼ 0.05 is significance level and 1 ¼ 18 and 2 ¼ 1 are degrees of freedom). Poisoning caused by edible species of mushrooms represented as much as 400 ( p ¼ 87.53%) of the cases of all the poisonings and was significantly higher than poisoning caused by mushrooms having toxins equal to 57 ( p¼ 12.47%, F ¼ 2300.211, Fa12 ¼ 3.851, a ¼ 0.05, 1 ¼ 1, and 2 ¼ 1). The amount of poisoning caused by A. mellea was equal to 53 ( p ¼ 11.6% of all the poisoning), while all the other percentages of poisoning caused by every other edible species of mushroom were usually less than 9%. Finally, among the species with toxins the highest incidences were found for A. phalloides group poisoning (N ¼ 40, p ¼ 8.75%), in relation to all of the poisoning cases (Table 1). Statistical analysis of data dealing with different methods of mushrooms gaining were performed at a confidence interval of p ¼ 0.95. The results are shown in Table 2. We found that the percentages of the methods of mushroom gaining used by the poisoned patients possessed statistically significant differences (F ¼ 456.524, Fa12 ¼ 2.614, a ¼ 0.05, 1 ¼ 3, and 2 ¼ 1). Independent mushroom collection was the most frequent method of mushroom collection for poisoning patients ( p ¼ 71%). The data concerning the circumstances of collection, transport, and storage of mushrooms as well as storage of mushroom dishes are presented in Table 3. The analysis revealed that the percentages of the long-term storage of mushroom dishes ( p ¼ 28.75), collecting and storing them in plastic bags ( p ¼ 25.25), and a long period of storing the collected mushrooms ( p ¼ 21.75) possessed statistically significant differences (F ¼ 32.766, Fa12 ¼ 2.223, a ¼ 0.05, 1 ¼ 5, and 2 ¼ 1).
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Table 3. Poisoning caused by edible mushroom species depends on circumstances of mushroom collection, transport, and storage. Circumstance
N
p [%]
Long-term storage of mushroom dishes 115 28.75 (>2 days) Collection and storage in plastic bags 101 25.25 Long period of storage of the collected 87 21.75 mushrooms (>2 days) High air temperature during harvesting 38 9.50 (25 C) Old and mechanically damaged mushrooms 31 7.75 Long period of transport at high temperature 28 7.00 (>3 h, 25 C) N: number of poisoning, p: percentage of circumstances of mushrooms collection, transport and storage [%], n ¼ 400 of the total poisoning cases caused by edible species.
In Table 4, the data on the occurrence of poisoning caused by mushrooms as recorded by the DCT in Krakow was compared to those recorded by the RCAPS.11 The percentage of poisoning caused by edible mushrooms recorded in the years 2003–2007 by the RCAPS ( p ¼ 79.08%) was higher than the percentage of mushrooms that have defined the toxin ( p ¼ 20.92%) (F ¼ 327.145, Fa12 ¼ 3.851, a ¼ 0.05, 1 ¼ 1, and 2 ¼ 1). At the DCT in Krakow, the percentage of edible mushroom poisonings was higher than the analogous in Sosnowiec for about 8.5 percentage points (Table 4).
Discussion In the case of mushroom poisoning an important diagnostic factor is the interval between the intake of the dish and the occurrence of manifestations from the gastrointestinal tract. Hepatotoxic mushrooms, for example, the A. phalloides group, trigger initial gastrointestinal symptoms after 6 h. An appropriate account of this history of this taken from the patient is also extremely important. Early diagnosis and the identification of the mushroom species are of substantial prognostic significance.1,4 A lack of mushroom identification may complicate the management of the poisoned patient.2 Unfortunately, in most cases, mycological analysis is impossible to provide immediately. As such, mushroom identification cannot delay the treatment. When interviewing patients suspected of mushroom poisoning, a detailed history concerning the ingestion should be obtained. The mushroom ingested is often difficult
Table 4. Comparison of the poisoning caused by both edible and toxic mushroom species recorded by the DCT in Krakow and The Regional Center of Acute Poisoning, Sosnowiec. Poisonings Krakow—present data Poisonings caused by edible mushrooms Poisonings caused by toxic mushrooms Sosnowiec (2003–2007) Poisonings caused by edible mushrooms Poisonings caused by toxic mushrooms
N
p [%]
400 57
87.53 12.47
253 67
79.08 20.92
N: number of poisoning; p: percentage of poisoning; n1 ¼ 457 and n2 ¼ 320 of the total poisoning cases (caused by both edible and toxic species) in Krakow and Sosnowiec respectively.
to identify, and the actual ingested mushroom is usually not available for examination. Attempts made to use systems for electronic identification based on reported characteristics have likewise been unsuccessful.3 If whole mushrooms or mushroom fragments are available, they should be saved for identification by an experienced mycologist. The latest annual report from the American Association of Poison Control Center (AAPCC) showed 6600 cases of exposure to mushrooms in 2012, but only 17% were identified by the species.15 Mushroom identification requires specialist expertise and is beyond the capabilities of health care professionals. The use of a method such as the Internet for the purpose of mushroom identification is wholly inadequate for untrained personnel. Incorrect identification could potentially impact on patient care.9 Also the verbal descriptions of mushrooms are subjective because the mushroom morphology can differ depending on the season, the stage of growth, local habitat, and environmental conditions.9,13 Photographic images are useful, but they are not a substitute for formal identification using actual specimens when such material is available.9 Analysis of mushroom spores detected in gastrointestinal contents allows for the determination of the mushroom species that may have caused the poisoning before any changes occur in other diagnostic parameters. The type of investigated material is also an important factor that can determine the validity of such studies. The highest importance is ascribed to samples of gastrointestinal contents rich in non digested food, when collected in the initial hours of poisoning. These include vomit and secured remnants of uneaten food and mushroom peelings. Such materials include entire
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fragments of sporocarps, which, when examined macroscopically and microscopically, reveal the morphological properties allowing prompt identification of the genus. Microscopic examination of the above materials is aimed at determining the presence of spores and spore identification via comparison with standard fungal spores. Our results describe the epidemiology of wild mushroom poisoning in the years 2002–2009 in Southeast Poland. In this study, we show that inquiries regarding mushroom poisoning amount to a relatively infrequent 2.53% reason for contacting the DCT in Krakow. Wild mushroom poisonings commonly occurred in autumn and summer, corresponding with the mushroom season in Poland (Figure 1). The biggest percentage of poisoning was connected with independent mushroom collection (Table 2). The suspicion of toxic mushroom species as a causative agent of poisoning seems obvious. However, our results show that the biggest percentage of poisoning is caused by edible species (Table 1). The relationship between poisoning percentages caused by toxic and edible species was similar in the RCAPS data (Table 4). The analysis of the circumstances of mushroom collection, transport, and storage shows that the largest percentage of poisoning was caused by long-term storage of mushroom dishes, collecting and storing in plastic bags, and long storage of mushrooms (Table 3). It should be emphasized that the main reason for edible mushroom poisoning is due to their incorrect processing after harvest (Table 3). There are some reports of mushroom poisoning from different parts of the world.2,7,9,11,12,13 Poisoning in the majority of cases was not serious from a clinical aspect. The most common symptoms were nausea, vomiting, abdominal pain, and diarrhea. The mainstay of therapy was symptomatic and supportive. Unfortunately, in most cases, it was not possible to determine the type of mushroom ingested by the patients, but some of them were edible species.2,11 The mushrooms contain choline, which as a result of autolysis transforms to toxic neurine (vinyltrimethyl-ammonium hydroxide CH2¼CHN(CH3)3 OH).16 The vomiting principles in an animal model of Rhodophyllus rhodopolius poisoning were connected with large amounts of choline, muscarine, and muscaridine.17 Scientific studies on neurine are few— with the most recent dating back to the mid-1950s. Neurine possesses muscarinic (M1) and nicotinic receptors’ agonist property.18
Edible mushroom species are known to have factors that could lead to a health disorder. Repeated meals, large amounts ingested, incorrect preparation, and ingestion of raw mushrooms may lead to severe symptoms.2,9,12 Gastroenteritis can be induced by edible mushroom species containing large amounts of mucus; for example, the sticky bum, S. luteus, and fragments of this mushroom can remain in the stomach even for 3 days while manifesting symptoms of gastritis.19 The gastrointestinal disturbances may result from the low activity of trehalase in the small intestine mucosa. Trehalase is a glycoside hydrolase enzyme which catalyses the conversion of trehalose to glucose.20 The results of our observations indicate additional, but so far not yet described, factors. As indicated in the patient form,14 the fruit bodies of these mushrooms were mechanically damaged during transportation or were stored 2 days or more prior to consumption. Our study included 457 patients diagnosed with mushroom poisoning based on the history provided by the patients, symptoms, physical examination, and laboratory tests. The analysis revealed that 12.47% of the patients were poisoned with mushrooms containing specific toxins such as cyclopeptides, muscarine, psilocybin, muscimol/ibotenic acid, and gastrointestinal irritants (Table 1). In 87.53% of the patients, nausea, vomiting, stomach ache or diarrhoea occurred within 30 min to 4 h after the ingestion of the edible mushrooms. Laboratory testing did not show any significant abnormalities. The edible species that induced poisoning most frequently were the honey mushroom, the parasol mushroom, the sticky bum, the chanterelle, and the field mushroom (Table 1). The results of the epidemiological data, from RCAPS, indicated that the most frequent cases of poisoning were caused by edible mushrooms, with usually little effect.11 The same method for mushroom identification was used by us and RCAPS enabling comparison of the data with our results. Unfortunately, detailed medical history concerning mushroom collection, transport, and storage and proceeding with mushroom dish were not conducted in RCAPS. The main limitation of the study is its retrospective character. The DCT is a tertiary referral centre. In some cases, when the species of mushrooms were known and the course of poisoning mild, patients were treated in different hospitals in our region. This accounts for the selection bias in this study. Moreover pernicious vomiting causes the stomach to empty, leading to the gastric contents being poor in spores.
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This resulted in spore identification being impossible in 38 cases. The pediatric cases of mushroom poisoning were not analyzed, thus significantly impoverishing the study.
Conclusions Based on spore analysis of the gastric content, edible mushrooms were responsible for the great majority of mushroom poisoning cases admitted to the DCT. The toxicity of edible mushroom is associated with proceeding with them during collection, transport, and storage. The medical history should be supplemented by questions concerning these circumstances. The identification of the mushroom by a mycologist is highly desirable. Conflict of interest The authors declared no conflicts of interest.
Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
References 1. Karlson-Stiber C and Persson H. Cytotoxic fungi—an overview. Toxicon 2003; 42: 330–339. 2. Schenk-Jaeger KM, Rauber-Lu¨thy C, Bodmer M, et al. Mushroom poisoning: a study on circumstances of exposure and patterns of toxicity. Eur J Inter Med 2012; 23: 85–91. 3. Beuhler MC, Sasser HC and Watson WA. The outcome of North American pediatric unintentional mushroom ingestions with various decontamination treatments: an analysis of 14 years of TESS data. Toxicon 2009; 53: 437–443. 4. Lampe KF. Pharmacology and therapy of mushroom intoxication. In: Rumack BH and Salzman E (eds) Mushroom Poisoning: Diagnosis and Treatment. BocaRaton, FL: CRC Press, 1978, pp. 125–169. 5. Wu YQ and Sun CY. Poison control services in China. Toxicol 2004; 198: 279–284. 6. Lima DA, Costa Fortes R, Gabri Novaes MRC, et al. Poisonous mushrooms; a review of the most common intoxications. Nutr Hosp 2012; 27: 402–408. 7. Pajoumand A, Shadnia S, Efricheh H, et al. A retrospective study of mushroom poisoning in Iran. Hum Exp Toxicol 2005; 24: 609–613.
8. Tegzes JH and Puschner B. Toxic mushrooms. Vet Clin North Am Small Anim Pract 2002; 32: 397–407. 9. Cassidy N, Duggan E and Tracey JA. Mushroom poisoning in Ireland: the collaboration between the National poisons information centre and expert mycologists. Clin Toxicol (Phila) 2011; 49: 171–176. 10. Berger KJ and Guss DA. Mycotoxins revisited: Part II. J Emerg Med 2005; 28: 175–183. 11. Kapala M, Nowacka A, Kicka M, et al. Mushroom (Fungi) poisoning investigated at the regiolan centre of acute poisoning, institute of occupational medicine and environmental health, Sosnowiec, Poland. Probl Forensic Sci 2008; LXXV: 282–293. 12. Kintziger KW, Mulay P, Watkins S, et al. Wild mushroom exposures in Florida, 2003-2007. Public Health Rep 2011; 126: 844–52. 13. Nordt SP, Manoguerra A and Clark RF. 5-Year analysis of mushroom exposures in California. The West J Med 2000; 173: 314–317. 14. Satora L. Non-specific mushroom poisoning. Vet Hum Toxicol 2004; 46: 224. 15. Mowry JB, Spyker DA, Cantilena LR, et al. 2012 Annual report of the American association of poison control centers’ National Poison Data System (NPDS): 30th annual report. Clin Toxicol (Phila) 2013; 51: 949–1229. 16. Williams EF Jr, Hoffman CF and Nash TP Jr. Stimulation of gastric secretion by neurine. Am J Physiol 1943; 139: 364–365. 17. Maki T, Takahasi K and Shibata S. Isolation of vomiting principles from the mushroom Rhodophyllus rhodopolius. J Agric Food Chem 1985; 33: 1204–1205. 18. Tweedie D, Brossi A, Chen D, et al. Neurine, an acetylocholine autolysis product, elevates secreted amyloid- protein precursor and amyloid- peptide levels, and lowers neuronal cell viability in culture: a role in Alzheimer’s disease? J Alzheimers Dis 2006; 10: 9–16. 19. Prager MH and Goos RD. A case of mushroom poisoning from Suillus luteus. Mycopathol 1984; 3: 175–176. 20. Arola H, Koivula T, Karvonen AL, et al. Low trehalase activityis associated with abdominal symptoms caused by edible mushrooms. Scand J Gastroenterol 1999; 34: 898–903.
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Edible mushroom-related poisoning: A study on circumstances of mushroom collection, transport, and storage
Human and Experimental Toxicology 1–7 ª The Author(s) 2014 Reprints and permission: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0960327114557901 het.sagepub.com
T Gawlikowski1, M Romek2 and L Satora3
Abstract Background: The American Association of Poison Control Center (AAPCC) shows that in 2012 there were 0.3% of human exposures involving mushrooms. Only 17% of 6600 cases were then identified by the species. The present retrospective study was designed to identify the epidemiology of mushroom poisoning in adults admitted to Krakow’s Department of Clinical Toxicology (DCT) from 2002 to 2009. Materials and Methods: This study was conducted retrospectively after examining the files of 457 adult patients with wild mushroom poisoning. Mycological analysis was made and the species of the poisoninginducing mushroom was determined. Furthermore, the circumstances related to the mushroom gathering, transport, storage, preparation, and consumption have been analyzed. Results: The analysis revealed that in 400 (87.53%) out of 457 cases, the clinical symptoms were caused by ingestion of identified edible mushroom species. The main reason for edible mushroom poisoning is associated with their incorrect processing after harvest. The analysis of the circumstances of mushroom collection, transport, and storage shows that the largest percentage of poisoning was connected with long-term storage of mushroom dishes, collecting, and storing them in plastic bags, and long storage of mushrooms. Conclusion: Based on spore analysis of the gastric content, edible mushrooms were responsible for the great majority of mushroom poisoning cases admitted to the DCT. The toxicity of edible mushroom is associated with proceeding with them during collection, transport, and storage. The medical history should be supplemented by questions concerning these circumstances. The identification of the mushroom by a mycologist is highly desirable. Keywords Edible mushroom poisoning, epidemiology, mycologist
Introduction The gathering and consumption of wild mushrooms is a traditional social outing in Europe, Asia, and the United States. 1–5 Mushrooms were described also as popular remedies in ancient oriental documents, and some of them became ingredients in traditional medicine.6 The consumption of wild mushrooms is very popular in Poland. An estimated figure of over 10 million Poles participate in mushroom hunts each year, and from 18,000 to 20,000 tons of wild mushrooms are harvested annually, usually for personal consumption. From about 10,000 species of mushroom about 50–100 species are poisonous.7 It is important to note that the most mushroomderived toxins poisonous to humans are resistant to
cooking, canning, freezing, or any other processing method. Therefore, the only way to avoid poisoning is to avoid consumption of the toxic species. There are
1
Department of Clinical Toxicology, Jagiellonian University Medical College, Krakow, Poland 2 Department of Cytology and Histology, Institute of Zoology Jagiellonian University, Krakow, Poland 3 Department of Physiology and Reproduction of Animals, University of Rzeszow, Rzeszow, Poland Corresponding author: T Gawlikowski, Department of Clinical Toxicology, Jagiellonian University Medical College, ul. Sniadeckich 10, Krakow, 31501, Poland. Email: [email protected]
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no universal clinical care guidelines for the cases of mushroom poisoning. The choice of treatment is guided by the clinical symptoms, and for most mushroom toxins there is no antidote.8 Modern methods of intensive care medicine have reduced mushroom mortality and morbidity substantially.1,4 The diagnosis of mushroom poisoning should be based on mushroom identification, clinical features, and laboratory analyses.9 Mushrooms have numerous spores characteristic for each species.10,11 The gastric contents, the reminder of a mushroom dish, and the whole mushrooms themselves are subject to evaluation. Most literature related to mushroom exposures and poisonings are clinical case reports, with few studies characterizing the epidemiology of exposures.12 Additionally, in medical literature, there are studies investigating exposure to toxic mushrooms and subsequent hospitalizations in the United States3,12,13 but comparable studies in Europe appear seldom, to our knowledge.2,9 The observations supported by data in the literature indicated edible species as the most common cause of mushroom poisoning.2,11 Since edible mushrooms do not have specific toxins, what is the cause of their toxicity? The preliminary study led us to believe that the circumstances of mushroom collection, transport, and storage might be related to the edible mushroom poisonings.14 The study group consists of wild mushroom-poisoned adult patients admitted to the Department of Clinical Toxicology (DCT), Jagiellonian University Medical College in Krakow, Poland. In each case of mushroom poisoning, the detailed interview concerning the proceeding with mushroom during and after collection, and the mushroom dish was done.14 The specialist mycologist made a spore analysis of the gastric contents and identified mushroom species. We performed this study to present descriptive epidemiological data on mushroom enquiries to the DCT in Krakow, with particular attention to the circumstances of their collection, transportation, and storage. The results have been compared with literature data.11
Materials and methods This study was conducted retrospectively after examining the files of adult (18 years and older) patients with wild mushroom poisoning who were admitted to the DCT from 2002 to 2009. The referral population, in Southeast Poland, amounts to about 7 million
people. Demographic and detailed clinical information on exposure cases, circumstances of poisoning, symptoms, and the causality are recorded in a systematic and standardized manner by a physician trained in clinical toxicology. On admission to the DCT, the form concerning the circumstances related to the mushroom gathering, transport, storage, preparation, and consumption was completed.14 A detailed history was taken from each patient. The database was reviewed by one doctor specializing in clinical toxicology. The diagnosis of mushroom poisoning was based on the history provided by the patients, symptoms, and physical examination. The laboratory tests conducted included blood analysis namely electrolytes (sodium and potassium), creatinine, glucose, alanine aminotransferase, aspartate aminotransferase, creatine kinase, total bilirubin, blood cell counts (red blood cells, white blood cells, hematocrit, hemoglobin, and platelets), and prothrombin time expressed as the international normalized ratio index. Additionally, when Amanita phalloides poisoning was suspected, urine analysis used for amanitin was conducted. Patients with co-ingestion of drugs in overdose or drugs of abuse, affected by diseases of the digestive system, and subjects treated with medicine that might affect gastrointestinal function were not enrolled. Febrile patients were excluded from the study because of infection suspicion, which could be responsible for reported complaints. In all of the included cases, the specialist mycologist made a spore analysis of the gastric contents. Microscopic examination of the gastric contents is aimed at determining the presence of spores and spore identification. The species of the poison-inducing mushroom was determined in all included cases. Spore analysis was made with the use of a light microscope (type Olympus BX 50-F, Japan). Two microscopic specimens were made, one stained with Lugol’s solution, while the other one was not stained. The spores were evaluated at a magnification of 400. The spores that were found were identified using atlases and then compared with the model spores—specimens of spores of a specific mushroom species. The spore models were obtained from mushrooms collected and identified by a specialist mycologist. The dried model sporocarps of mushrooms, containing spores, were stored in sealed containers. The preparation of the model spores was conducted at the same time as the mycological analysis of spores obtained from a poisoned patient. All the preparations were stained in the same way.
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Figure 1. Monthly variation for cases of mushroom poisoning reported to the Department of Clinical Toxicology in the years 2002–2009.
The results were compared with data that referred the mushroom species responsible for poisoning from the Regional Centre of Acute Poisoning in Sosnowiec (RCAPS), Southwest Poland, with 10 million population.11 The same methods of spore analysis were used by RCAPS. The statistical analysis was performed using the STATISTICA data analysis software system, version 10 (StatSoft. Inc. 2011). We calculated the percentage p of poisoning caused by different edible and toxic species as well as the percentage of poisoning caused by the mushroom collection method and the percentage of poisoning under different circumstances concerning the collection of the mushrooms, their transport, and their storage as a ratio for the total number of poisoned people by edible species only. The differences between the analyzed groups were detected using a Fisher–Snedecor test. The present retrospective study was designed to identify the epidemiology of mushroom poisoning in adults from 2002 to 2009. Furthermore, the circumstances of mushroom collection, transport, and storage have been analyzed.
Results We identified 457 patients poisoned by wild mushrooms (mean age 43.81 + 18.53 years; 62.8% female) during the study period, among a total of 18,043 poisoning cases, where the frequency of wild mushroom poisoning was 2.53%. Apart from
mushrooms that contain psychoactive toxins, the ingestion of toxic mushrooms was accidental and caused by misidentification of species. August, September, and October were the peak months for mushroom poisoning (Figure 1), and these months are generally warm and rainy. In 400 ( p ¼ 87.53%) out of 457 cases, the mycological analysis revealed that the clinical symptoms were caused by ingestion of identified edible mushroom species (Table 1). The symptoms of patients with edible mushroom poisoning were vomiting ( p ¼ 82%), nausea ( p ¼ 68%), abdominal discomfort ( p ¼ 58%), and diarrhoea ( p ¼ 38%), and they occurred within 30 min to 4 h of the intake of a dish containing the mushrooms and subsided after 1–3 days. During that time, laboratory tests did not reveal any significant abnormalities. In all of the cases, gastric lavage and a single dose of charcoal were administrated (1 g kg1 body weight). On the first day of the treatment, a light diet was initiated, and the water and electrolyte imbalance was compensated intravenously, if necessary. Only isotonic fluids were used for intravenous infusions. Saline was preferred. When the gastrointestinal symptoms subsided, the diet limitations were lifted. No laxatives, antiemetics, or antidiarrhoeal medication were administered. The duration of the treatment was 1–3 days. In 21 cases (5.25%), the patients were hospitalized when pernicious vomiting and colliquative diarrhoea occurred. The edible mushroom species identified as the most
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Table 1. Poisoning caused by different species of mushrooms (edible and toxic) observed by the DCT in the years 2002–2009. Mushroom
N
p [%]
Edible species Armillariella mellea (Vahl) P. Kumm.1871 53 11.60 Physalacriaceae Macrolepiota procera (Scop.) Singer 1948 39 8.53 Agaricaceae Suillus luteus (L.) Roussel 1796 Suillaceae 37 8.10 Cantharellus cibarius Fr. 1821 Cantharellaceae 36 7.88 Agaricus campestris L. 1753 Agaricaceae 35 7.66 Xerocomus (Boletus) badius (Fr.) Fr. 1832 28 6.13 Boletaceae Russula virescens (Schaeff.) Fr. 1836 28 6.13 Russulaceae Boletus edulis Bull. 1782 Boletaceae 22 4.81 Lactarius deliciousus (L.) Gray 1821 Russulaceae 22 4.81 Leccinum aurantiacum (Bull.) Gray 1821 21 4.59 Boletaceae Tricholoma equestre (L.) P. Kumm. 1871 21 4.59 Tricholomataceae Clitocybe gibba (Pers.) P. Kumm. 1871 20 4.38 Tricholomataceae Marasmius oreades (Bolton) Fr. 1836 19 4.16 Marasmiaceae Leccinum scabrum (Bull.) Gray 1821 Boletaceae 19 4.16 Sum 400 87.53 Toxic species Amanita phalloides group 40 8.75 Hallucinogenic mushrooms 12 2.62 Boletus satanas Lenz 1831 Boletaceae 2 0.44 Hypholoma fasciculare (Huds.) P. Kumm 1871 2 0.44 Strophariaceae Entoloma sinuatum (Bull.) P. Kumm.1871 1 0.22 Entolomataceae Sum 57 12.47 DCT: Department of Clinical Toxicology in Krakow. N: number of poisoning; p: percentages of poisoning [%] of the total poisoning caused by both, edible and toxic species; n ¼ 457 total cases of poisoning.
common causes for poisoning were the honey mushroom Armillariella mellea, the parasol mushroom Macrolepiota procera, the sticky bum Suillus luteus, the chanterelle Cantharellus cibarius, the field mushroom Agaricus campestris, the Bay Bolete Boletus badius, and the green-cracking Russula Russula virescens (Table 1). The results of the mycological analysis are reported in Table 1. These analyses were carried out among patients of DCT in the years 2002–2009. It was shown that the incidences of poisonings were caused by both edible and toxic species of mushrooms. Statistically significant differences existed between the percentages
Table 2. The mushroom gaining method used by poisoned patients of the DCT in the years 2002–2009. Methods of mushroom gaining Independent mushroom collection Purchase from a person near road Purchase at market Purchase in a shop
N
p [%]
284 54 44 18
71.00 13.50 11.00 4.50
DCT: Department of Clinical Toxicology in Krakow. N: number of poisoning; p: percentage of the mushrooms gaining methods used by poisoned patients by edible species only [%]; n ¼ 400 of the total poisoning cases caused by edible species.
of poisoning caused by different mushroom species (value of the Fisher–Snedecor statistics F ¼ 8.74, critical value of the Fisher–Snedecor statistics Fa12 ¼ 1.614, where a ¼ 0.05 is significance level and 1 ¼ 18 and 2 ¼ 1 are degrees of freedom). Poisoning caused by edible species of mushrooms represented as much as 400 ( p ¼ 87.53%) of the cases of all the poisonings and was significantly higher than poisoning caused by mushrooms having toxins equal to 57 ( p¼ 12.47%, F ¼ 2300.211, Fa12 ¼ 3.851, a ¼ 0.05, 1 ¼ 1, and 2 ¼ 1). The amount of poisoning caused by A. mellea was equal to 53 ( p ¼ 11.6% of all the poisoning), while all the other percentages of poisoning caused by every other edible species of mushroom were usually less than 9%. Finally, among the species with toxins the highest incidences were found for A. phalloides group poisoning (N ¼ 40, p ¼ 8.75%), in relation to all of the poisoning cases (Table 1). Statistical analysis of data dealing with different methods of mushrooms gaining were performed at a confidence interval of p ¼ 0.95. The results are shown in Table 2. We found that the percentages of the methods of mushroom gaining used by the poisoned patients possessed statistically significant differences (F ¼ 456.524, Fa12 ¼ 2.614, a ¼ 0.05, 1 ¼ 3, and 2 ¼ 1). Independent mushroom collection was the most frequent method of mushroom collection for poisoning patients ( p ¼ 71%). The data concerning the circumstances of collection, transport, and storage of mushrooms as well as storage of mushroom dishes are presented in Table 3. The analysis revealed that the percentages of the long-term storage of mushroom dishes ( p ¼ 28.75), collecting and storing them in plastic bags ( p ¼ 25.25), and a long period of storing the collected mushrooms ( p ¼ 21.75) possessed statistically significant differences (F ¼ 32.766, Fa12 ¼ 2.223, a ¼ 0.05, 1 ¼ 5, and 2 ¼ 1).
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Table 3. Poisoning caused by edible mushroom species depends on circumstances of mushroom collection, transport, and storage. Circumstance
N
p [%]
Long-term storage of mushroom dishes 115 28.75 (>2 days) Collection and storage in plastic bags 101 25.25 Long period of storage of the collected 87 21.75 mushrooms (>2 days) High air temperature during harvesting 38 9.50 (25 C) Old and mechanically damaged mushrooms 31 7.75 Long period of transport at high temperature 28 7.00 (>3 h, 25 C) N: number of poisoning, p: percentage of circumstances of mushrooms collection, transport and storage [%], n ¼ 400 of the total poisoning cases caused by edible species.
In Table 4, the data on the occurrence of poisoning caused by mushrooms as recorded by the DCT in Krakow was compared to those recorded by the RCAPS.11 The percentage of poisoning caused by edible mushrooms recorded in the years 2003–2007 by the RCAPS ( p ¼ 79.08%) was higher than the percentage of mushrooms that have defined the toxin ( p ¼ 20.92%) (F ¼ 327.145, Fa12 ¼ 3.851, a ¼ 0.05, 1 ¼ 1, and 2 ¼ 1). At the DCT in Krakow, the percentage of edible mushroom poisonings was higher than the analogous in Sosnowiec for about 8.5 percentage points (Table 4).
Discussion In the case of mushroom poisoning an important diagnostic factor is the interval between the intake of the dish and the occurrence of manifestations from the gastrointestinal tract. Hepatotoxic mushrooms, for example, the A. phalloides group, trigger initial gastrointestinal symptoms after 6 h. An appropriate account of this history of this taken from the patient is also extremely important. Early diagnosis and the identification of the mushroom species are of substantial prognostic significance.1,4 A lack of mushroom identification may complicate the management of the poisoned patient.2 Unfortunately, in most cases, mycological analysis is impossible to provide immediately. As such, mushroom identification cannot delay the treatment. When interviewing patients suspected of mushroom poisoning, a detailed history concerning the ingestion should be obtained. The mushroom ingested is often difficult
Table 4. Comparison of the poisoning caused by both edible and toxic mushroom species recorded by the DCT in Krakow and The Regional Center of Acute Poisoning, Sosnowiec. Poisonings Krakow—present data Poisonings caused by edible mushrooms Poisonings caused by toxic mushrooms Sosnowiec (2003–2007) Poisonings caused by edible mushrooms Poisonings caused by toxic mushrooms
N
p [%]
400 57
87.53 12.47
253 67
79.08 20.92
N: number of poisoning; p: percentage of poisoning; n1 ¼ 457 and n2 ¼ 320 of the total poisoning cases (caused by both edible and toxic species) in Krakow and Sosnowiec respectively.
to identify, and the actual ingested mushroom is usually not available for examination. Attempts made to use systems for electronic identification based on reported characteristics have likewise been unsuccessful.3 If whole mushrooms or mushroom fragments are available, they should be saved for identification by an experienced mycologist. The latest annual report from the American Association of Poison Control Center (AAPCC) showed 6600 cases of exposure to mushrooms in 2012, but only 17% were identified by the species.15 Mushroom identification requires specialist expertise and is beyond the capabilities of health care professionals. The use of a method such as the Internet for the purpose of mushroom identification is wholly inadequate for untrained personnel. Incorrect identification could potentially impact on patient care.9 Also the verbal descriptions of mushrooms are subjective because the mushroom morphology can differ depending on the season, the stage of growth, local habitat, and environmental conditions.9,13 Photographic images are useful, but they are not a substitute for formal identification using actual specimens when such material is available.9 Analysis of mushroom spores detected in gastrointestinal contents allows for the determination of the mushroom species that may have caused the poisoning before any changes occur in other diagnostic parameters. The type of investigated material is also an important factor that can determine the validity of such studies. The highest importance is ascribed to samples of gastrointestinal contents rich in non digested food, when collected in the initial hours of poisoning. These include vomit and secured remnants of uneaten food and mushroom peelings. Such materials include entire
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fragments of sporocarps, which, when examined macroscopically and microscopically, reveal the morphological properties allowing prompt identification of the genus. Microscopic examination of the above materials is aimed at determining the presence of spores and spore identification via comparison with standard fungal spores. Our results describe the epidemiology of wild mushroom poisoning in the years 2002–2009 in Southeast Poland. In this study, we show that inquiries regarding mushroom poisoning amount to a relatively infrequent 2.53% reason for contacting the DCT in Krakow. Wild mushroom poisonings commonly occurred in autumn and summer, corresponding with the mushroom season in Poland (Figure 1). The biggest percentage of poisoning was connected with independent mushroom collection (Table 2). The suspicion of toxic mushroom species as a causative agent of poisoning seems obvious. However, our results show that the biggest percentage of poisoning is caused by edible species (Table 1). The relationship between poisoning percentages caused by toxic and edible species was similar in the RCAPS data (Table 4). The analysis of the circumstances of mushroom collection, transport, and storage shows that the largest percentage of poisoning was caused by long-term storage of mushroom dishes, collecting and storing in plastic bags, and long storage of mushrooms (Table 3). It should be emphasized that the main reason for edible mushroom poisoning is due to their incorrect processing after harvest (Table 3). There are some reports of mushroom poisoning from different parts of the world.2,7,9,11,12,13 Poisoning in the majority of cases was not serious from a clinical aspect. The most common symptoms were nausea, vomiting, abdominal pain, and diarrhea. The mainstay of therapy was symptomatic and supportive. Unfortunately, in most cases, it was not possible to determine the type of mushroom ingested by the patients, but some of them were edible species.2,11 The mushrooms contain choline, which as a result of autolysis transforms to toxic neurine (vinyltrimethyl-ammonium hydroxide CH2¼CHN(CH3)3 OH).16 The vomiting principles in an animal model of Rhodophyllus rhodopolius poisoning were connected with large amounts of choline, muscarine, and muscaridine.17 Scientific studies on neurine are few— with the most recent dating back to the mid-1950s. Neurine possesses muscarinic (M1) and nicotinic receptors’ agonist property.18
Edible mushroom species are known to have factors that could lead to a health disorder. Repeated meals, large amounts ingested, incorrect preparation, and ingestion of raw mushrooms may lead to severe symptoms.2,9,12 Gastroenteritis can be induced by edible mushroom species containing large amounts of mucus; for example, the sticky bum, S. luteus, and fragments of this mushroom can remain in the stomach even for 3 days while manifesting symptoms of gastritis.19 The gastrointestinal disturbances may result from the low activity of trehalase in the small intestine mucosa. Trehalase is a glycoside hydrolase enzyme which catalyses the conversion of trehalose to glucose.20 The results of our observations indicate additional, but so far not yet described, factors. As indicated in the patient form,14 the fruit bodies of these mushrooms were mechanically damaged during transportation or were stored 2 days or more prior to consumption. Our study included 457 patients diagnosed with mushroom poisoning based on the history provided by the patients, symptoms, physical examination, and laboratory tests. The analysis revealed that 12.47% of the patients were poisoned with mushrooms containing specific toxins such as cyclopeptides, muscarine, psilocybin, muscimol/ibotenic acid, and gastrointestinal irritants (Table 1). In 87.53% of the patients, nausea, vomiting, stomach ache or diarrhoea occurred within 30 min to 4 h after the ingestion of the edible mushrooms. Laboratory testing did not show any significant abnormalities. The edible species that induced poisoning most frequently were the honey mushroom, the parasol mushroom, the sticky bum, the chanterelle, and the field mushroom (Table 1). The results of the epidemiological data, from RCAPS, indicated that the most frequent cases of poisoning were caused by edible mushrooms, with usually little effect.11 The same method for mushroom identification was used by us and RCAPS enabling comparison of the data with our results. Unfortunately, detailed medical history concerning mushroom collection, transport, and storage and proceeding with mushroom dish were not conducted in RCAPS. The main limitation of the study is its retrospective character. The DCT is a tertiary referral centre. In some cases, when the species of mushrooms were known and the course of poisoning mild, patients were treated in different hospitals in our region. This accounts for the selection bias in this study. Moreover pernicious vomiting causes the stomach to empty, leading to the gastric contents being poor in spores.
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This resulted in spore identification being impossible in 38 cases. The pediatric cases of mushroom poisoning were not analyzed, thus significantly impoverishing the study.
Conclusions Based on spore analysis of the gastric content, edible mushrooms were responsible for the great majority of mushroom poisoning cases admitted to the DCT. The toxicity of edible mushroom is associated with proceeding with them during collection, transport, and storage. The medical history should be supplemented by questions concerning these circumstances. The identification of the mushroom by a mycologist is highly desirable. Conflict of interest The authors declared no conflicts of interest.
Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
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8. Tegzes JH and Puschner B. Toxic mushrooms. Vet Clin North Am Small Anim Pract 2002; 32: 397–407. 9. Cassidy N, Duggan E and Tracey JA. Mushroom poisoning in Ireland: the collaboration between the National poisons information centre and expert mycologists. Clin Toxicol (Phila) 2011; 49: 171–176. 10. Berger KJ and Guss DA. Mycotoxins revisited: Part II. J Emerg Med 2005; 28: 175–183. 11. Kapala M, Nowacka A, Kicka M, et al. Mushroom (Fungi) poisoning investigated at the regiolan centre of acute poisoning, institute of occupational medicine and environmental health, Sosnowiec, Poland. Probl Forensic Sci 2008; LXXV: 282–293. 12. Kintziger KW, Mulay P, Watkins S, et al. Wild mushroom exposures in Florida, 2003-2007. Public Health Rep 2011; 126: 844–52. 13. Nordt SP, Manoguerra A and Clark RF. 5-Year analysis of mushroom exposures in California. The West J Med 2000; 173: 314–317. 14. Satora L. Non-specific mushroom poisoning. Vet Hum Toxicol 2004; 46: 224. 15. Mowry JB, Spyker DA, Cantilena LR, et al. 2012 Annual report of the American association of poison control centers’ National Poison Data System (NPDS): 30th annual report. Clin Toxicol (Phila) 2013; 51: 949–1229. 16. Williams EF Jr, Hoffman CF and Nash TP Jr. Stimulation of gastric secretion by neurine. Am J Physiol 1943; 139: 364–365. 17. Maki T, Takahasi K and Shibata S. Isolation of vomiting principles from the mushroom Rhodophyllus rhodopolius. J Agric Food Chem 1985; 33: 1204–1205. 18. Tweedie D, Brossi A, Chen D, et al. Neurine, an acetylocholine autolysis product, elevates secreted amyloid- protein precursor and amyloid- peptide levels, and lowers neuronal cell viability in culture: a role in Alzheimer’s disease? J Alzheimers Dis 2006; 10: 9–16. 19. Prager MH and Goos RD. A case of mushroom poisoning from Suillus luteus. Mycopathol 1984; 3: 175–176. 20. Arola H, Koivula T, Karvonen AL, et al. Low trehalase activityis associated with abdominal symptoms caused by edible mushrooms. Scand J Gastroenterol 1999; 34: 898–903.
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