Fungal Diversity (2014) 64:123–131 DOI 10.1007/s13225-013-0260-7

Investigation and analysis of 102 poisoning cases in Southern China from 1994 to 2012

Zuohong Chen & Ping Zhang & Zhiguang Zhang

Received: 17 June 2013 /Accepted: 31 July 2013 /Published online: 15 August 2013 # Mushroom Research Foundation 2013

Abstract is the main cause of mortality Keywords Mushroom poisoning . . Syndrome . in food poisoning incidents in China. Although some respon- Psilocybe samuiensis . Rhabdomyolysis sible mushroom species have been identified, some were identified inaccuratly. This study investigated and analyzed 102 mushroom poisoning cases in southern China from 1994 Introduction to 2012, which involved 852 patients and 183 deaths, with an overall mortality of 21.48 %. The results showed that 85.3 % Approximately 3,800 species of have been of poisoning cases occurred from June to September, and catalogued in China, and about 421 species are considered involved 16 species of poisonous mushroom: Amanita species as poisonous (Mao 2000, 2006). Collecting wild mushrooms (A. fuliginea, A. exitialis, A. subjunquillea var. alba, A. cf. for human consumption has been a long-standing tradition in pseudoporphyria, A. kotohiraensis, A. neoovoidea, A. many areas in southern China. However, edible and poisonous gymnopus), Galerina sulciceps, Psilocybe samuiensis, mushrooms may be frequently confused, or their identities subnigricans, R. senecis, R. japonica, Chlorophyllum mistaken, leading to an annual toll of mushroom poisoning molybdites, involutus, Leucocoprinus cepaestipes incidents. The statistical data of the national food poisoning and Pulveroboletus ravenelii. Six species (A. subjunquillea report from the Chinese Center for Control and Pre- var. alba, A. cf. pseudoporphyria, A. gymnopus, R. japonica, vention (CDC) showed that 311 mushroom poisoning events Psilocybe samuiensis and Paxillus involutus) are reported for were reported, with 1,954 poisoning cases and 409 deaths. the first time in poisoning reports from China. Psilocybe The mortality was 20.93 % where mushroom poisoning was samuiensis is a newly recorded species in China. The genus the main cause of death (Niu et al. 2011; Jin and Li 2009). Amanita was responsible for 70.49 % of fatalities; the main However, most of the investigations and reports from the lethal species were A. fuliginea and A. exitialis. Russula CDC focused on epidemiology, and the reports from hospitals subnigricans caused 24.59 % of fatalities, and five species mainly emphasized the syndromes (Niu et al. 2011; Jin and Li showed mortality >20 % (A. fuliginea, A. exitialis, A. 2009;Yuetal.2012;Zhouetal.2009;Chenetal.1991). subjunquillea var. alba, R. subnigricans and Paxillus Identification of which mushrooms were responsible for the involutus). Mushroom poisoning symptoms were classified poisoning events is often inaccurate. For example, before from among the reported clinical symptoms. Seven types of 2005, most of the lethal species belonging to Amanita genus mushroom poisoning symptoms were identified for clinical were identified as A. phalloides, A. verna and A. virosa (Li diagnosis and treatment in China, including gastroenteritis, et al. 2002;Chenetal.1991). In recent years, acute liver failure, acute renal failure, psychoneurological experts in China investigated mushroom poisoning cases or disorder, , rhabdomyolysis and photosensitive identified the mushrooms responsible for the incidents. The dermatitis. results indicated that some poisonous mushrooms (especially in the genus Amanita) did not occur in Europe or in North America, and some are new species or belong exclusively to East Asian taxa (Yang 2000a, 2005). For example, A. exitialis, * : : Z. Chen ( ) P. Zhang Z. Zhang which caused 52 poisoning cases including 20 fatalities during College of Life Sciences, Hunan Normal University, – Changsha 410081, China 2000 2010 (Deng et al. 2011), has only been reported in e-mail: [email protected] Guangdong Province (Yang 2005). Amanita fuliginea, which 124 Fungal Diversity (2014) 64:123–131 caused many fatal poisoning cases in Hunan and Jiangxi and collected from the field and eaten at home in the Provinces (Zhang et al. 2002; Huang et al. 2002), occurs only remaining 101 cases; therefore, the data should reflect the in China and Japan (Yang 2005). A “little white mushroom” natural occurrence of the mushrooms over time. Table 1 which caused about 400 sudden unexplained deaths in Yun- shows that 85.30 % of the poisoning cases, 91.31 % of nan Province during summers over the last 35 years has been poisoned patients and 84.70 % of deaths occurred from June identified as a new species, venenata (Yang et al. to September. These periods are hot and rainy in southern 2012). In this paper, we report the investigation and analysis China, which are suitable conditions for the rapid growth of of 102 mushroom poisoning cases in southern China from wild mushrooms. The seven cases that occurred in March and 1994 to 2012, clarifying the mushroom species responsible April were in Guangdong Province, where the climate is and their clinical symptoms. warmer and wetter than other parts of southern China.

Materials and methods Poisonous mushroom species

Sourcesofmaterials Sixteen species of poisonous mushrooms were identified by morphological, anatomical and molecular studies. The results We collected the mushroom poisoning specimens from the are shown in Table 2, and some of them are displayed in field and clinical symptoms data from the hospital records of Fig. 1. Among them, seven species belong to the genus the poisoned patients in southern China, including Hunan, Amanita: A. fuliginea Hongo, A. exitialis Zhu L. Yang & T. Hubei, Guangdong, Jiangxi, Guizhou, Chongqing and Si- H. Li, A. subjunquillea var. alba Zhu L. Yang, A. cf. chuan Provinces, from 1994 to 2012. pseudoporphyria Hongo, A. kotohiraensis Nagas. & Mitani, A. neoovoidea Hongo and A. gymnopus Corner & Bas. Three Mushroom identification species of the genus Russula were identified: R. subnigricans Hongo, R. senecis S. Imai and R. japonica Hongo. The other The mushroom specimens were collected from the scene of six species were Galerina sulciceps (Berk.) Boedijn, the poisoning accidents and confirmed by the patients or their Chlorophyllum molybdites (G. Mey.) Massee, Leucocoprinus family members. The mushrooms were identified by morpho- cepaestipes (Sow.: Fr.) Pat., Pulveroboletus ravenelii (Berk. & logical and anatomical studies, and molecularly by internal M.A. Curtis) Murrill, Psilocybe samuiensis Guzmán, Bandala transcribed spacer sequence analysis. All specimen vouchers & J.W. Allen and Paxillus involutus (Batsch) Fr. For six were deposited at the Herbarium of College of Life Sciences, species (A. subjunquillea var. alba, A. cf. pseudoporphyria, Hunan Normal University (MHHNU). A. gymnopus, R. japonica, Psilocybe samuiensis and Paxillus involutus), this is the first report of their involvement in Data analysis poisoning in China. Psilocybe samuiensis is a newly recorded

EXCEL 2003 was used to establish a database for statistical analysis. Table 1 Monthly distribution of mushroom poisoning

Month No. of Percent No. of Percent No. of Percent cases (%) patients (%) deaths (%) Results Jan. 0 0 0 0 0 0 Overview of mushroom poisoning Feb. 0 0 0 0 0 0 Mar.5 4.90273.17147.65 One hundred and two mushroom poisoning cases were inves- Apr.2 1.96131.5384.37 tigated in southern China from 1994 to 2012. Seventy-eight May 2 1.96 6 0.70 3 1.64 cases occurred in Hunan Province, and 24 in Chongqing, June 45 44.12 316 37.09 83 45.35 Guangdong, Guizhou, Hubei, Jiangxi, and Sichuan Provinces, July 14 13.73 85 9.98 21 11.48 which involved 852 poisoned patients with 183 patient deaths, Aug. 18 17.65 136 15.96 37 20.22 giving a mortality of 21.48 %. Sept. 10 9.80 241 28.28 14 7.65 Oct. 2 1.96 4 0.47 2 1.09 Monthly distribution of mushroom poisoning Nov.3 2.94172.0010.55 Dec. 1 0.98 7 0.82 0 0 Except for one incident where the patients ate dried mush- total 102 100 852 100 183 100 rooms at a restaurant, the poisonous mushrooms were fresh Fungal Diversity (2014) 64:123–131 125

Fig. 1 Poisonous mushrooms found in southern China. A. Amanita fuliginea;B.A. exitialis; C. A. subjunquillea var. alba;D. A. cf. pseudoporphyria;E.A. kotohiraensis;F.A. gymnopus;G. Galerina sulciceps;H.Russula subnigricans;I.Russula japonica;J.Chlorophyllum molybdites;K.Pulveroboletus ravenelii;L.Psilocybe samuiensis

species in China, and this is the first report of R. japonica in Paxillus involutus was caused by the ingestion of a single mainland China. species. However, in the poisoning cases induced by A. Table 2 shows that 64.70 % of poisoning cases, 78.05 % of fuliginea and A. subjunquillea var. alba, most of the cases poisoned patients and 70.49 % of deaths were caused by the were caused by the ingestion of miscellaneous mushroom species of the genus Amanita. Among the genus Amanita,the species, most of which could be edible; however, because of main lethal species were A. fuliginea and A. exitialis.In carelessness, the collection and ingestion of A. fuliginea or A. addition, 13.73 % of the poisoning cases, 10.33 % of poisoned subjunquillea var. alba caused the poisoning. In eight of the patients and 24.59 % of deaths were caused by R. 33 cases caused by A. fuliginea, where the poisoning was subnigricans. The combined poisoning cases, patients and caused by ingestion of A. fuliginea only, mortality was 60– deaths caused by these three fatal mushrooms were 51.96 %, 100 %. 55.63 % and 78.69 %, respectively. Table 2 also shows that eight of the mushroom species Monthly distribution of poisoning cases caused by different could cause fatalities. Among them, five species had a mor- mushrooms tality >20 %: A. fuliginea, A. exitialis, A. subjunquillea var. alba, R. subnigricans and Paxillus involutus. The mortality Different mushroom species grow during different seasons, data should be explained here. In our investigation, we found and understanding the periods when the poisoning occurred that the poisoning induced by A. exitialis, R. subnigricans and would help prevent and diagnose mushroom poisoning. 126 Fungal Diversity (2014) 64:123–131

Table 2 Toxic mushroom species causing poisoning in southern China

Mushroom species No. of cases Percent (%) No. of patients Percent (%) No. of deaths Percent (%) Mortality (%)

Amanita fuliginea 33 32.35 352 41.32 79 43.17 22.44 A. exitialis 6 5.88 33 3.87 20 10.93 60.61 A. subjunquillea var. alba 3 2.94 13 1.53 4 2.19 30.77 A. cf. pseudoporphyria 3 2.94 22 2.58 4 2.19 18.18 A. kotohiraensis 2 1.96 91 10.68 1 0.54 1.10 A. neoovoidea 5 4.90 15 1.76 2 1.09 13.33 A. gymnopus 1 0.98 4 0.47 0 0 0 Other Amanita species 13 12.75 135 15.84 19 10.38 14.07 Galerina sulciceps 1 0.98 1 0.12 0 0 0 Russula subnigricans 14 13.73 88 10.33 45 24.59 51.14 R. senecis 1 0.98 5 0.59 0 0 0 R. japonica 1 0.98 3 0.35 0 0 0 Chlorophyllum molybdites 3 2.94 9 1.06 0 0 0 Leucocoprinus cepaestipes 1 0.98 5 0.59 0 0 0 Pulveroboletus ravenelii 1 0.98 22 2.58 0 0 0 Psilocybe samuiensis 4 3.92 24 2.81 0 0 0 Paxillus involutus 1 0.98 3 0.35 2 1.09 66.67 Other mushrooms 9 8.83 27 3.17 7 3.83 30.43 Total 102 100 852 100 183 100

Table 3 shows that poisoning cases caused by A. exitialis poisoning cases occurred from July to September and the occurred in March and April and A. fuliginea from April to Psilocybe samuiensis poisoning cases occurred in November September(butmostlyinJune).OtherAmanita poisoning and December. The other mushrooms poisoning cases oc- cases occurred from June to September. The R. subnigricans curred from May to October.

Table 3 Monthly distribution of poisoning cases caused by different mushrooms

Mushroom species Mar. April May June July Aug. Sept. Oct. Nov. Dec. Total

Amanita fuliginea 1 1 26 4 1 33 A. exitialis 51 6 A. subjunquillea var. alba 21 3 A. cf. pseudoporphyria 11 1 3 A. kotohiraensis 11 2 A. neoovoidea 23 5 A. gymnopus 11 Other Amanita species 7 5 1 13 Galerina sulciceps 11 Russula subnigricans 48 2 14 R. senecis 11 R. japonica 11 Chlorophyllum molybdites 11 1 3 Leucocoprinus cepaestipes 1 Pulveroboletus ravenelii 11 Psilocybe samuiensis 314 Paxillus involutus 11 Other mushrooms 5 3 1 9 Total 5 2 2 45 14 18 10 2 3 1 102 Fungal Diversity (2014) 64:123–131 127

Ecological environment of poisonous mushrooms growth latent stage, which lasted approximately to 6–12 h after inges- tion and no symptoms appeared, the second stage was gastro- Among these poisonous mushrooms, all species in the genus enteritis characterized by the acute onset of nausea and Amanita and Russula, Pulveroboletus ravenelii and Paxillus vomiting, diarrhea, abdominal pain or electrolyte abnormali- involutus are ectomycorrhizal fungi, which mainly grow in ties and dehydration, this stage lasted 12–24 h. During the broad-leaved forests and mixed forests, consisting of third, recovery, stage, the patient felt better for 12–24 h, before Pinaceae, Fagaceae, Betulaceae and Salicaceae. Some poison- deteriorating during the fourth stage, which was characterized ous mushrooms form with more specific higher by dramatic rises in liver transaminases (ALT, AST), which plants; for example, A. fuliginea mainly occurs in broad- caused liver and renal failure, and multi-organ exhaustion. leaved forests consisting of Castanopsis and Lithocarpus. A. Death usually occurred within 5–8 days post-ingestion. exitialis mainly occurs in forests consisting of Castanopsis Among the Amanita species, the symptoms caused by A. fissa. The other poisonous mushrooms are mainly saprophyt- pseudoporphyria, A. neoovoidea and A. gymnopus were dif- ic. Among them, G. sulciceps grows on rotten wood or on ferent from those of A. fuliginea and A. exitialis. The liver piles of sawdust. Chlorophyllum molybdites, L. cepaestipes transaminases did not increase significantly, but acute renal and Psilocybe samuiensis mainly grow in fields fertilized with failure did occur and some patients died suddenly within 4– manure. 6 days post-ingestion. Patients poisoned with R. subnigricans presented gastroin- Clinical symptoms of different poisonous mushrooms testinal symptoms, such as nausea and vomiting, diarrhea and abdominalpain,within2hafteringestion.Chesttightness, The clinical symptoms data were obtained from the hospital dyspnea, generalized muscle pain followed after 6–12 h, se- records of the poisoned patients and are shown in Table 4.All vere patients presented with hematuria or hemoglobinuria and species, except Psilocybe samuiensis, caused gastrointestinal significantly elevated creatine kinase levels, which led to symptoms, including nausea and vomiting, diarrhea, and ab- rhabdomyolysis and acute renal failure, with death occurring dominal pain, accompanied by dizziness, headache and weak- within 12–24 h post-ingestion. ness. Gastrointestinal symptoms occurred alone within 30 min Psilocybe samuiensis caused psychoneurological disor- to 3 h after ingesting mushrooms species including C. ders: the patients presented with emotional instability, visual molybdites, R. senecis, R. japonica, L. cepaestipes and hallucinations and disturbance of consciousness within Pulveroboletus ravenelii. Ingestion of these species did not 30 min to 1 h after ingestion, but could return to normal after lead to death. Poisoning by species in the genus Amanita and 3–5 h. A patient described blue mushrooms dangling in the G. sulciceps appeared over four stages: the first stage was the dark in front of his eyes.

Table 4 Clinical symptoms of different poisonous mushrooms

Mushroom species Gastroenteritis Acute liver failure Acute renal failure Psychoneurological disorder Hemolysis Rhabdomyolysis

Amanita fuliginea ✓✓ A. exitialis ✓✓ A. subjunquillea var. alba ✓✓ A. cf. pseudoporphyria ✓✓ A. kotohiraensis ✓✓ A. neoovoidea ✓✓ A. gymnopus ✓✓ Other Amanita species ✓✓ G. sulciceps ✓✓ R. subnigricans ✓✓ ✓ R. senecis ✓ R. japonica ✓ C. molybdites ✓ L. cepaestipes ✓ Pulveroboletus ravenelii ✓ Psilocybe samuiensis ✓ Paxillus involutus ✓ ✓ 128 Fungal Diversity (2014) 64:123–131

Mushroom poisoning with hemolytic symptoms occurred 2005. Since the late 1990s, Dr. Yang and his research group in Hexin town of Deyang, Sichuan Province, in September, members have performed a systematic study of samples of the 2004. The causative mushroom was identified as Paxillus genus Amanita collected from all over China. The results involutus. The patients presented with nausea and vomiting, revealed that many collections were misidentified: the Euro- diarrhea and abdominal pain within 2–4 h after ingestion, pean or North American rarely occurred in East followed by onset of acute , hemoglobinuria and ure- Asia, and the Amanita species in East Asia were unique and mia, finally leading to liver and and death 36 h had their own geographical ranges (Yang 1997, 2000a, b, after ingestion. 2005; Yang and Zhang 2002; Zhang et al. 2004). Several new poisonous species, including A. fuligineoides P. Zhang & Zhu L. Yang, A. pallidorosea P. Zhang & Zhu L. Yang and Discussion A. rimosa P. Zhang & Zhu L. Yang, which were collected in recent years, are also endemic to East Asia (Zhang et al. 2010). Species and geographical distribution of poisonous Our study indicated that all of the poisonous Amanita species mushrooms were endemic to East Asia, and they are distributed in China, Japan, Singapore, South Korea, India and Nepal (Yang 2005). Fatal mushroom poisoning has long been recognized as a Among them, the lethal A. fuliginea and A. subjunquillea var. major human health hazard worldwide. There are many mush- alba occurred only in China and Japan, and the lethal A. room poisoning incidents in Europe, North America and Asia exitialis has only been identified in Guangdong Province, each year. It is estimated that 100–200 fatalities per year are China. caused by mushroom poisoning in the United States and Some of the species identified in our investigation are Europe (Ellenhorn and Barceloux 1988; Mengs et al. 2012). distributed worldwide, including C. molybdites, Paxillus Yamaura (2013) reported the latest mushroom poisoning data involutus, L. cepaestipes and Pulveroboletus ravenelii;how- from 2001 to 2010 in Japan: the total incidents of mushroom ever, others are endemic to Asia. For example, G. sulciceps is poisoning were 569 cases, involving 1,920 patients and 10 distributed in tropical Indonesia and India (Boedijn 1938)and deaths. The species of poisonous mushrooms in Europe and R. subnigricans is mainly distributed in Japan and China North America have been identified by studies of a large (Imazeki and Hongo 1989;Mao2000). Russula japonica number of poisoning incidents in past decades. The results was first reported in Japan (Imazeki and Hongo 1989)andis have been summarized in certain classic books and reviews also distributed in Taiwan (Zhou and Zhang 2005); the present (Benjamin 1995; Bresinsky and Besl 1990; Spoerke and study is the first record of its discovery in mainland China. Rumack 1994; Berger and Guss 2005a, b; Christine and Hans Psilocybe samuiensis was first found in Koh Samui, a small 2003). Benjamin (1995) thought that 400 of 10,000 species of tropical island in Thailand (Guzmán et al. 1993), and until mushrooms may be poisonous, with 20 poisonous species now, has never been seen in China. being common and less than six species being lethal. In Although poisonous mushrooms are abundant in China, Europe and North America, more than 90 % of all fatal and mushroom poisoning cases are frequent, the actual poi- mushroom poisonings were caused by the genus Amanita sonous mushrooms responsible were seldom identified. In (Bresinsky and Besl 1990), the main species were A. addition to the 16 species of poisonous mushrooms identified phalloides, A. verna and A. virosa (Christine and Hans in our investigation, the main poisonous mushrooms identi- 2003;Wieland1986; Enjalbert et al. 2002). fied by mycologists include A. pallidorosea (Cao et al. 2011), Wild mushrooms resources are abundant and collecting A. subjunquillea var. alba, which are frequently misidentified wild mushrooms is popular in China. Although there were as A. verna or A. virosa (Yang 2005), Trogia venenata (Yang some mushrooms poisoning incidents, few reports were et al. 2012), Lampteromyces luminescens M. Zang and L. recorded before 1980. The scientific identification and classi- japonicus (Kawam.) Singer (Weng et al. 1991), Cordierites fication of poisonous mushrooms began rather late; the book frondosa (Kobayasi) Korf (Liu and Yang 1992), Boletus “Poisonous Mushrooms” edited by the Mycologist Group of venenatus Nagas., B. sinicus W. F. Chiu and B. magnificus Institute of Microbiology, Chinese Academy of Sciences W. F. Chiu (Sun et al. 2012), Chiua virens (W.F.Chiu)Y.C. (1975) recorded 83 species of poisonous mushrooms. The Li & Z. L. Yang, Heimioporus retisporus (Pat. & C. F. Baker) book “The Identification to Poisonous Mushrooms” edited E. Horak, Tylopilus eximius (Peck) Singer and T. microspores by Mao (1987) recorded 183 species of poisonous mush- S. Z. Fu, Q. B. Wang & Y. J. Yao (Li et al. 2011), Inocybe rooms. In China, before the 1990s, the identification of mush- rimosa (Bull.) P. Kumm. and I. fastigiata (Schaeff.) Quél. rooms, especially the genus Amanita, used the names of (Sheng 1981), and I. asterospora Quél. (Chen et al. 1987), species in Europe and North America because science and Psilocybe Cubensis (Earle) Singer and Panaeolus retirugis technology was underdeveloped at the time. This phenome- (Fr.) Gillet (He and Ma 2001). Most of these poisonous non persisted for some macrofungus flora and literature until mushrooms were new species and are endemic to East Asia. Fungal Diversity (2014) 64:123–131 129

Toxins of the lethal mushrooms cooked fruitbodies cause gastrointestinal poisoning (Bresinsky and Besl 1990). Paxillus involutus also causes This investigation indicated that there were five identified immunohemolytic anemic cases, termed Paxillus syndrome, lethal Amanita species in southern China that could cause which is believed to be due to an of the mushroom that death, comprising A. fuliginea, A. exitialis, A. subjunquillea stimulates the formation of an immune complex which sec- var. alba, A. cf. pseudoporphyria and A. neoovoidea.Our ondarily attaches itself to the surface of erythrocyte to cause previous studies demonstrated that the α-amanitin and β- agglutination and haemolysis (Flammer 1985; Winkelmann amanitin contents in the fruitbodies of A. fuliginea, A. exitialis et al. 1986). In many areas of China, P. involutus are used as and A. subjunquillea var. alba are high: the total amatoxins edible mushrooms, and when raw, cause gastrointestinal reached 10350.70, 6921.90 and 792.5 μgg−1 dried symptoms (Mao 2000). The poisoning caused by P. involutus fruitbodies, respectively (Chen et al. 2003;Huetal.2012). with hemolytic symptoms recorded here is the first report in Amanitins are responsible for deaths that occur from ingestion China. of these mushrooms. They are thermostable bicyclic octapep- Previous studies showed that the hemolytic activity of P. tides that inhibit RNA polymerase II, blocking the synthesis of involutus is caused by immunological reactions (Flammer proteins and leading to cell death. Acute liver failure is the 1985;Winkelmannetal. 1986). However, Habtemariam characteristic symptom of amatoxin poisoning (Wieland (1996) demonstrated that the fresh fruitbodies of P. involutus 1986;Nguyenetal.1996; Rudd and Luse 1996). contained a non-polar, acid- and thermo-stable cytotoxic com- Although the amanitin contents of the fruitbodies of A. cf. ponent that may contribute to the observed hemolytic and pseudoporphyria, A. neoovoidea and A. gymnopus are very low other clinical manifestations of Paxillus poisoning. However, or absent (Chen et al. 2003), they may cause acute renal failure or the toxic component has not yet been identified. lead to death. However, the symptoms are different from those caused by A. fuliginea or A. exitialis. and A. Symptoms of mushroom poisoning proxima in Europe and North America, and A. pseudoporphyria in Japan have been recorded as causing acute renal failure since The toxins in different poisonous mushrooms are not the same, 1992; the responsible toxin is probably 2-amino-4,5-hexadienoic but the same toxin generates the same poisoning symptoms. acid (Warden and Benjamin 1998; Saviuc and Danel 2006; Thus, mushroom poisoning symptoms were mainly classified Iwafuchi et al. 2003). This toxin was also identified in A. abrupt according to the mushroom toxins in many studies before 2000. (Yamaura et al. 1986), A. neoovoidea (Hatanaka and Kawakami For example, Koppel (1993) distinguished seven different types 1980), A. gymnopus (Hatanaka 1992)andA. miculifera of mushroom poisoning: (1) phalloides, (2) orellanus, (3) (Hatanaka et al. 1998). Recently, Kirchmair et al. (2012)reported gyromitra, (4) muscarine, (5) pantherina, (6) psilocybin, and three poisoning cases caused by A. boudieri, A. gracilior and A. (7) gastrointestinal mushroom syndrome. Two other types of echinocephala with symptoms of acute renal failure. The A. adverse reaction to mushrooms are (8) coprinus and (9) paxillus smithiana toxin was detected in these three Amanita species syndrome. Spoerke and Rumack (1994) divided the poisoning using thin layer chromatography. The structure of this toxin is symptoms into seven groups: (1) Cyclopeptides, (2) Ibotenic similar to the lethal toxin isolated from Trogia venenata, a novel acid, (3) Monomethylhydrazine, (4) Muscarine-histamine, (5) poisonous species that has caused hundreds of sudden unexpect- Coprine, (6) Hallucinogenic indoles and (7) Gastrointestinal ed deaths in Yunnan Province, China, over the last 30 years (Shi irritants. However, several new mushroom poisoning syn- et al. 2012; Zhou et al. 2012;Yangetal.2012). dromes, including acute renal failure induced by A. smithiana, Previous studies on the constituents of R. subnigricans report- A. proxima and A. pseudoporphyria; erythromelalgia syndrome ed six chlorinated phenylethers designated as russuphelins A, B, described with acromelalga and C. amoenolens; C, D, E and F. Of these compounds, russuphelins A, B, C and D rhabdomyolysis caused by Tricholoma equestre and R. exhibited cytotoxic activity (Takahashi et al. 1992, 1993). Sev- subnigricans; and encephalopathy after ingestion of eral cases of fatal poisoning with distinctive symptoms of rhab- Hapalopilus rutilans and Pleurocybella porrigens have been domyolysis caused by R. subnigricans occurred in Japan from described since the early 1990s (Saviuc and Danel 2006). In a 2005 to 2007. Matsuura et al. (2009) identified the genuine toxic recent review on mushroom poisoning syndromes, Diaz (2005) R. subnigricans and isolated the responsible toxin, guided by summarized an expanded syndromic classification of mush- lethal toxicity in mice through oral injection. A small, highly room poisoning, based on presentation time and target organ strained carboxylic acid cycloprop-2-ene carboxylic acid was systemic toxicity, using the data of 28,018 cases of global isolated from the toxic R. subnigricans. This compound is re- mushroom poisoning. The 14 major syndromes were stratified sponsible for fatal rhabdomyolysis; the LD100 value in mice was first by presentation time and then by target organ systemic 2.5mgkg−1. toxicity and included early (<6 h), late (6–24 h), and delayed Paxillus involutus is one of the three most common causes syndromes (>1 day). There were eight early syndromes (four of poisoning by mushrooms in Europe. 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