Poisonous mushrooms; a review of the most common intoxications

Hongos venenosos; una revisión de las intoxicaciones más comunes

A. D. L. Lima¹, R. Costa Fortes², M. R.C. Garbi Novaes³ and S. Percário⁴

¹Laboratory of Experimental Surgery. University of Brasilia-DF. Brazil/Paulista University-DF. Brazil.
²Science and Education School Sena Aires-GO/University of Brasilia-DF/Paulista University-DF. Brazil.
³School of Medicine. Institute of Health Science (ESCS/FEPECS/SESDF)/University of Brasilia-DF. Brazil. ]]> ⁴Institute of Biological Sciences. Federal University of Pará. Brazil.

Correspondence

ABSTRACT

Mushrooms have been used as components of human diet and many ancient documents written in oriental countries have already described the medicinal properties of fungal species. Some mushrooms are known because of their nutritional and therapeutical properties and all over the world some species are known because of their toxicity that causes fatal accidents every year mainly due to misidentification. Many different substances belonging to poisonous mushrooms were already identified and are related with different symptoms and signs. Carcinogenicity, alterations in respiratory and cardiac rates, renal failure, rhabidomyolisis and other effects were observed in toxicity studies with various species including edible and therapeutic ones. Proper identification is important to avoid accidents and toxicity studies are necessary to assure the safe use of mushrooms as food and for medicinal purposes.

Key words: Toxicity. Mushrooms. Toxins. Review.

RESUMEN

Las setas se han utilizado como componentes de la dieta humana y muchos documentos antiguos escritos en los países orientales se han descrito ya las propiedades medicinales de las especies de hongos. Algunos hongos son conocidos por sus propiedades nutricionales y terapéuticas y de todo el mundo, algunas especies son conocidas debido a su toxicidad que causa accidentes mortales cada año, principalmente debido a errores de identificación. Muchas sustancias diferentes que pertenecen a las setas venenosas estaban ya clasificadas y están relacionados con diferentes síntomas y signos. Carcinogenicidad, alteraciones de la frecuencia respiratoria y cardiaca, insuficiencia renal, rhabidomyolisis y otros efectos se observaron en estudios de toxicidad con varias especies incluidas las alimenticias y terapéuticas. La correcta identificación es importante para evitar accidentes y los estudios de toxicidad son necesarias para asegurar el uso seguro de las setas como alimento y con fines medicinales.

Palabras clave: Toxicidad. Hongos. Toxinas. Revisión.

Introduction

Approximately 140.000 species of mushrooms have already been catalogued all over the world, about 2.000 being considered safe for human consumption and about 700 have therapeutic properties.¹ A great variety of species was classified as poisonous and represents risks to health if ingested. Apart from mushrooms that contain psychoactive toxins, ingestion of toxic mushrooms is invariably accidental and caused by misidentification of species.^2,3

There are some mushrooms that contain exceptionally powerful toxins that represent a real hazard to health even when ingested in small doses. Most toxins were well studied and are described in literature, such as amatoxins that are cytotoxic and cause harm to kidney and liver and orellanine that is nephrotoxic.²

Some species are well utilized for food and medicine due to the presence of pharmacologically active substances and essential nutrients. Because of these properties, mushrooms were described as popular remedies in ancient oriental documents and some of them became ingredients in traditional medicine.^4,5,6 Even in species with beneficial properties toxic substances were already found.⁷

Before using species of mushroom for human consumption it is necessary to characterize their toxicological profile because even in some edible species toxic substances have been identified. The toxicity studies consist of exposing species of mammal to a toxic agent during a specific period of time.⁸ The aim of the present work is to review the most common intoxications caused toxic species and the toxic potential caused by edible and medicinal mushrooms.

Poisonous species of mushrooms

Some species of mushrooms are known as toxic and in some countries many cases of mushroom poisoning are reported every year. In the year 1998 in France 1,675 cases of intoxications by mushrooms were reported and in this country alone it is estimated that 8-10.000 cases are expected to be registered every year. Most of these accidents are due to incorrect identification of species that is often made by empirical and traditional knowledge.^3,9 A wide variety of toxic mushrooms belong to different genus that will be discussed bellow.

Genus Amanita

Other toxins also found in Amanita genus belong to the family of phallotoxin that includes phalloin, phalloidin, phallisin, phallacidin, phallacin and phallisacin. Virotoxin is also found in this genus and are closed related the phallotoxins.¹⁰

The specie A. phalloides is responsible for the majority of the fatalities caused by mushroom poisoning. The toxic effects are caused by phallotoxin and amatoxin. Phallotoxin causes alterations of enterocytes cellular membrane, while amatoxin inhibits protein synthesis at a transcriptional level within enterocytes, hepatocytes and proximal renal tubular cells. After ingestion of A. phalloides, amatoxin causes necrosis of liver cells with mortality rates ranging from about 10% to 20%. Only a minority of patients need emergency liver transplantation.^11,12

Species with hallucinogenic effects are also found in amanita genus. A. pantherina and A. muscaria are well known toxic mushrooms that have been mistaken for the edible mushroom A. rubescens. Two dissociative constituents such as ibotenic acid (IBO) and muscimol (MUS) are responsible for the hallucinogenic effects. IBO is a powerful agonist of N-methyl-D-aspartic-acid (NMDA) receptor and MUS is a potent GABAA agonist.¹³ The intoxications caused by A. muscaria for long time were believed to be due to muscarine, but it was demonstrated that this substance is present in small amounts.¹⁴

A. muscaria and A. pantherina grow in North America, Europe, Africa and Japan, in recent years it has been reported that young people in several countries have intentionally eaten A. muscaria to evoke hallucinations. ¹⁵ The most common symptoms of intoxication are motor depression, ataxia, changes in mood, perception and feelings, dizziness, euphoria, drowsiness, gastrointestinal disturbances and muscle twitches.^13,15,16

The pantherina-muscaria syndrome is atropine-like and in the number and severity of poisoning cases fatality is rare. In most cases recovery is complete after 24 hours. The treatment is mainly symptomatic cholinestarase inhibitors may be recommended as it counteracts the effects of poisoning, benzodiazepinics or phenobarbitone can be used in case of seizures.^14,17 The treatment of patients intoxicated with species containing amatoxins includes detoxification, careful monitoring and sometimes liver transplantation is necessary.¹⁰

Genus Clitocybe and Inocybe

A particular syndrome that affected five people in the region of Savoie in France was later identified as intoxication caused by the mushroom Clitocybe amoenolens. First symptoms appeared 24 hours after ingestion. Patients presented paresthesia of the toes and fingers followed by paroxysmal burning pain lasting 2-3 hours, notably at night. A sensation of heat, numbness, oedema and local erythema are associated with crises. Symptoms are partially relieved with cold water, acetylsalicylic acid, morphine and clomipramine. Recovery is completely after 1-4 months.¹⁸

The administration of high dose of C. amoenolens in rats caused weight loss, locomotor disability and erythema of the toes. Examination of the sciatic nerves showed decreased axon density and neuronal fiber degeneration.¹⁹

The poisonous specie C. acromelalga can be confused with the edible one Lepista inversa. The substances pointed out as responsible for the symptoms are the acromelic acids A-E. Acromelic acid (ACRO) is a kainate analogue that is assumed to be involved in poisoning episodes. ACRO has two isomers, ACROA, which is the most potent and ACRO-B. ACRO-A was demonstrated to have a powerful excitatory action on mechanosensitive unmyelinated afferents in skeletal muscle of the rat.²⁰

There are approximately 40 species belonging do Inocybe genus in China, and they are known to be not edible. The species: I. asterospora, I. fastigiata f. subcandida, I. gobeyi, I. lilacina, I. nappies, I. pallidicremea, I. patowillandii, I. radiate, I. repanda and I. rimosa have toxic properties. They produce neurotoxic and psychotropic effects due to the presence of biogenic amines, muscarin, aeruginacin a thymethylammonium analogue of psylocibin which effects will be discussed later in this article.²³ Intoxications caused by members of this genus is similar to the ones caused by Clitocybe because the species contain muscarine.³

Genus Cortinarius

The genus Cortinarius comprises between 2,000-3,000 species of mushrooms that were considered as non-toxic until 1950. One hundred-and-thirty-five cases of intoxication caused by C. orellanus were described from 1953-1962 in Poland. Poisoning syndrome is characterized by a delayed acute tubulopathy that can progress to chronic renal insufficiency. ²²

In several case reports it was demonstrated that the mushrooms C. speciosissimus and C. orellanus are nephrotoxic due to the presence of the cyclopeptide orellanine whose metabolites are supposed to be most active. In additional studies it was shown that the oxidation of orellanine in renal tissue may accumulate quinone compounds which bind covalently with biological structures leading to cell damage.²

The symptoms of orellanine intoxication may appear between 2-20 days after ingestion. Initially people can experience nausea, vomiting and abdominal pain. This is followed by intense thirst, chills, polyuria or oliguria and possibly anuria. Hemodialysis may be necessary until renal function gradually improves.²³

Some species of genus Cortinarius can be confused with members of Psilocybe genus which is known as magic because the hallucinogenic properties. This fact has led to several cases of accidental intoxication because Psilocybe mushrooms are used for some people for recreational purposes.²⁴

Genus Gyromitra

Species of genus Gyromitra, family Helvellaceae are really attractive to hunters and gourmets because of their taste. However, some species of Gyromitra contain a well known toxin named gyromitrin, whereas other species are non-toxic. This is one of the reasons why intoxications occur, toxic and non-toxic species are sometimes difficult to distinguish because they are mixed-up. The other reason is that the toxin is water soluble and volatile, boiling for long time and drying allows ingestion without risk of poisoning, but if these procedures are not done properly intoxication may occur.²

The third reason for intoxication is the confusion with species that are consumed frequently. The specie G. esculenta is known as false morels and is commonly confused with morels such as Morchella esculenta and M. elata. The toxin gyromitrin is the responsible for the effects of this specie. Intoxications have occurred not only by eating fresh false morels but also by the inhalation of vapors from cooking.^3,9

The other effect of gyromitrin include carcinogenesis due to the hepatic metabolization that produces free radicals with mutagenic properties in animals and are also responsible for the hepatic problems. Symptoms of intoxication start 8-12 hours after ingestion. Treatment consists of monitoring the symptoms and administrating vitamin B6 intravenously considering that gyromitrin inactivates this vitamin.²⁶

Genus Psilocybe

The use of psychoactive substances of fungal origin for recreational purposes has become an increasing problem in many countries all over the world. Species of genus Psilocybe are known due to their psychedelic effects caused by psilocybin.²⁷ Common psylocibin containing mushrooms are: P. semilanceata, P. Mexicana, P. bohemica, P. cubensis and P. baeocistis.²⁵

The symptoms of intoxication occur 30 minutes after ingestion of fresh or dried mushroom and start with anxiety, nausea, vertigo and asthenia, neurosensorial symptoms consists of visual problems, disorientation, motor incoordination and sympathomimetic symptoms consist of mydriasis, tachycardia and hypertension. Recovery is completely 4 to 12 hours after ingestion. The need of hospitalization is rare and in exceptional cases myocardial infarction may occur in adult patients while children may present hyperthermia, seizures and comma.²⁵

Toxicity caused by commonly consumed mushrooms

Some species known as edible and medicinal also have substances that can cause harm to health, but the dose and magnitude of effects on humans must be carefully studied. Ostreolysin is a cytolytic protein that was isolated from mushrooms of the genus Pleurotus that was able to cause cytolytic pore formation when administered by intravenous route to rats. As a consequence it was observed blood pressure increase, cardiac ischemia, tachycardia, hypoxia and elevated serum potassium.²⁸ (table 2)

The administration of the mushroom Phellinus linteus to rats bearing experimentally induced prostatic hyperplasia leads to an enlargement of prostate stroma which is involved in transforming growth factor-beta₁ (TGF-β₁) regulation. The prostate is known to be regulated by various growth factors. Among them the TGFs have been reported to play important role in prostate cell growth regulation. The administration of P. linteus increased the expression of TGF-β₁ compared to animals treated with placebo.²⁹

Agaricus bisporus is the most consumed mushroom world-wide but is has been pointed out as potentially carcinogenic due to the substantial amounts of aromatic hydrazines, an established class of direct-acting chemical carcinogens. Life-time administration of A. bisporus raw or baked to mice three days a week followed by balanced semi-synthetic diet for the remaining days, induced tumors in a number of tissues. The administration of the methanolic and aqueous extracts of this same mushroom is weakly mutagenic. The ethanolic extract of this mushroom is increased in the presece of fungal mammalian enzyme systems purified mushroom tyrosinase and rat hepatic citosol.^30,31

The specie Pleucybella porrigens popularly known as Sugihiratake is a white mushroom widely distributed in the mountain areas of Japan and is commonly used as ingredient to various processed foods, but this was pointed out as hazardous due to the presence of substances analogous to vitamin D that are able to cause cryptogenic encephalopathy in patients with renal failure.³²

Species of genus Tricholoma especially T. equestre (T. flavovirens), known as yellow tricholoma, has been implicated in 12 human poisonings causing a delayed rhabdomyolysis severe enough to be fatal in 3 cases reported in France. The symptoms were muscular weakness, fatigue and myalgias within 24-72 hours after ingestion. The substance responsible for toxic effects was not identified.²

T. equestre is a wild mushroom considered in Europe as a delicacy. Toxicity is observed after a consumption of considerable amounts of fresh mushroom which ranges from 100 to 400 g at 3 to 9 consecutive meals.³⁴

A neurological syndrome appears after the ingestion of the specie Hapalopilus rutilans that is considered edible. Common symptoms consist of visual disturbances, somnolence, hypotonia and hepatic and renal insufficiency.³⁵ Hepatic cytolysis and renal insufficiency were described in children.^22,36

Conclusion

In countries where mushrooms are highly consumed, a number of intoxications are reported every year mainly due to misidentification of species. Hazardous toxins are present in these species and are able to cause different syndromes that can be fatal depending on the amount ingested. Accidental ingestion of mushrooms is difficult to avoid especially in countries where eating wild species is common. Proper identification is important to avoid accidents and the identification of symptoms and signs of intoxication as soon as possible enables the success of treatment. Intoxications caused by commonly consumed mushrooms were already described, for this reason edible mushrooms and the ones having pharmacological potential must be carefully studied in order to identify the possibility of intoxications, so more studies have to be carefully conducted, clinical and experimental assays with medicinal species must investigate the side effects that may occur.

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Correspondence:
Renata Costa Fortes
Science and Education School Sena Aires-GO
University of Brasilia-DF/Paulista University-DF. Brazil
QI 14. CJ J. CS 26. Guara 1/DF. Brazil. CEP: 71.015-100
E-mail: renatacfortes@yahoo.com.br