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Gyromitra esculenta

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False Morel
Scientific classification
Kingdom:
Fungi
Phylum:
Ascomycota
Class:
Ascomycetes
Order:
Pezizales
Family:
Discinaceae
Genus:
Gyromitra
Species:
G. esculenta
Binomial name
Gyromitra esculenta
Gyromitra esculenta
View the Mycomorphbox template that generates the following list
Smooth hymenium
Cap is convex
Hymenium attachment is not applicable
Stipe is bare
Spore print is yellow to buff
Ecology is saprotrophic or mycorrhizal
Edibility is choice or deadly

Gyromitra esculenta is an ascomycete fungus from the genus Gyromitra widely distributed across Europe and North America, and one of several species of fungi known as False morels. It is normally found in sandy soils under coniferous trees in spring and early summer. The fruiting body, or mushroom, is an irregular brain-shaped cap dark brown in colour which can reach 10 cm (4 in) high and 15 cm (6 in) wide, perched on a stout white stalk up to 6 cm (2½ in) high.

Although Gyromitra esculenta is highly toxic and potentially fatal if eaten raw, it is described by aficionados as one of the best of all culinary mushrooms. It is popular in Scandinavia, Eastern Europe, and the upper Great Lakes region of North America. In Finland, it may be sold fresh, but it must be accompanied by warnings and instructions on correct preparation. Though it is still commonly consumed after parboiling, recent evidence suggests that even that procedure may not make the fungus entirely safe;[1] thus the organism's long-established classification as "edible and choice" is now disputed. When consumed, the false morel's principal active agent gyromitrin, is metabolized into the toxic compound monomethylhydrazine (MMH).

Taxonomy and naming

The fungus was first described by mycologist Christian Hendrik Persoon as Helvella esculenta in 1800,[2] before being placed in the genus Gyromitra by Fries in 1849, thus gaining its current accepted name.[3] The generic name is derived from the Greek terms gyros/γυρος 'round' and mitra/μιτρα 'headband'.[4] Its specific epithet is derived from the Latin esculentus, 'edible'.[5]

It is known by a variety of common names such as lorchel,[6] brain mushroom,[7] turban fungus,[8] elephant ears,[9] or beefsteak mushroom/morel.[10] The Finnish name Korvasieni is derived from the terms korva 'ear', and sieni 'mushroom/fungus',[11] [12] while the Swedish Stenmurkla is Sten 'stone' and murkla 'morel'.[13][14]

Gyromitra esculenta is a member of a family of fungi known as "False morels", named as such for their resemblance to the highly regarded true morels of the genus Morchella. The grouping also includes other species of the genus Gyromitra, such as G. infula (elfin saddle), G. caroliniana and G. gigas (Snow morel). While some of these species contain little to no gyromitrin, many sources recommend treating them all as poisonous, since their similar appearance and significant intraspecific variation can make reliable identification difficult. The more distantly related ascomycete mushrooms of the genus Verpa, such as V. bohemica and V. conica, are also known as false morels, early morels or thimble morels (and, like the Gyromitra, are also eaten by some and considered poisonous by others).[15]

Analysis of the ribosomal DNA of many of the Pezizales showed Gyromitra esculenta and the other false morels to be most closely related to the genus Discina, and also Pseudorhizina, Hydnotrya, and only distantly related to Helvella. Thus the four genera are now included in the family Discinaceae.[16]

Description

A younger specimen with a less wrinkled cap

The irregularly shaped cap may be up to 10 cm (4 in) high and 15 cm (6 in) wide. Initially smooth, it becomes progressively more wrinkled as it ages, resembling a brown brain when mature, and is attached to the stipe or stem at several points. The cap colour may be various shades of reddish-, chestnut-, purplish-, bay-, dark or sometimes golden-brown. Those from California have been reported as often more reddish-brown in colour.[7] The stipe is 3-6 cm (1¼-2½ in) high and 2-3 cm (1-1¼ in) wide, and is solid in this species unlike the hollow stipes of true morels.[17] The smell can be pleasant and has been described as fruity, and the fungus is mild-tasting. The spore print is whitish, with transparent spores elliptical and 17-22 μm in length.[18]

It is somewhat similar in appearance to the true morel (Morchella sp.), although the latter is more symmetric and looks more like a pitted gray, tan, or brown sponge. False morels (G. esculenta) are also generally darker and larger than true morels.[19]

Distribution and habitat

Gyromitra esculenta grows on sandy soil in coniferous and deciduous woodlands, although it prefers the former. Among conifers it is mostly found under pines (Pinus spp.), but also sometimes aspen (Populus spp.).[20] It is an early mushroom, and hunting period is from April to July, sometimes appearing with the melting snow.[7] It can be common in some years and rare in others. The mushroom is more commonly found in places where ground has been disturbed, such as openings, rivulets, washes, timber clearings, plowed openings, forest fire clearings, and roadsides.[17] The growth can be promoted by breaking the terrain further in places where false morel is known to grow.

Although more abundant in montane and northern coniferous woodlands such as the Sierra Nevada and the Cascade Range in northwestern North America, Gyromitra esculenta is found widely across the continent,[7] as well as being recorded from Mexico.[21] It is also common in Central Europe and less commonly in the east, and more montane areas than lowlands.[8] It has been recorded from Northern Ireland,[22] from Uşak Province in Western Turkey,[23] and from the vicinity of Kaş in the Antalya Province of Turkey's southern coast.[24]

Toxicity

Toxic reactions were known from the early 20th century at least, though the wide range in effects meant that some experts speculated the reaction was more of an allergic one related to the consumer, or misidentification, rather than innate toxicity of the fungus. Some would suffer severely or perish while others exhibited no symptoms after eating similar amounts of mushrooms from a single dish. Yet others would be poisoned after eating the mushroom for many years without ill-effects.[25] However, the fungus is now widely recognized as potentially deadly.[26]

Gyromitra esculenta contains the poisonous principle gyromitrin and although these mushrooms are only rarely involved in poisonings in either North America or Western Europe intoxications are seen frequently in eastern Europe and Scandinavia.[27] At one time up to 23% of mushroom fatalities each year were attributed to this species in Poland.[28] Deaths rates have now dropped; in Sweden poisoning is common but life-threatening poisonings have not been detected and there had not been a fatality reported over the 50 years from 1952 to 2002.[29]

A lethal dose of gyromitrin has been estimated to be between 10 to 30 mg/kg for children and 20 to 50 mg/kg in adults. These doses correspond to approximately to 0.2 to 0.6 kg and 0.4 to 1 kg of fresh mushroom respectively.[30] However, individual responses may vary and people who have ingested similar amounts may develop anything from minimal to severe toxicity.[31] There is evidence that children are more severely affected, and it is unclear whether this is due to a larger weight per body mass ratio consumed or that differences in enzyme and metabolic activity are responsible. [32] Although the amount of gyromitrin present can be significantly reduced through parboiling (leaching), it is a cumulative poison; there is evidence that repeated consumption can increase risk of toxicity.[31]

Geographical variation

Populations of Gyromitra esculenta appear to vary geographically in their toxicity. A French study has shown that mushrooms collected at higher altitudes have lower concentrations of toxin than those from lower elevations,[32] and there is anecdotal evidence fungi west of the Rocky Mountains in North America contain less toxin than those to the east.[33] However, poisonings in the west have been reported,[34] although they have been reported less frequently than the east.[35]

Biochemistry

MMH (CH3N2H3), a toxic metabolite also used in rocket fuel

The identity of the toxic constituents eluded researchers until 1968, when N-methyl-N-formylhydrazone acetaldehyde, better known as gyromitrin, was isolated.[36] Gyromitrin is a volatile water-soluble hydrazine compound metabolized in the body into monomethylhydrazine (MMH). MMH is a strongly reductive substance. [37] Other N-methyl-N-formylhydrazone derivatives have been isolated in subsequent research, although they are present in smaller amounts. These other derivatives likely also yield monomethylhydrazine when metabolized in the body. However, it remains unclear how much each contributes to the false morel's toxicity.[38]

The toxins react with pyridoxal-5-phosphate, which is the activated form of pyridoxine, forming a hydrazone. Overall this results in diminished formation of the neurotransmitter GABA via decreased activity of glutamic acid decarboxylase.[39] This interference causes the neurological symptoms. MMH also causes oxidative stress leading to methemoglobinemia.[30] Additionally during the metabolism of MMH, n-methyln-formylhydrazine is produced, this then undergoes cytochrome p450 regulated oxidative metabolism which via reactive nitrosamide intermediates leads to formation of methyl radicals which cause liver necrosis.[40][41] Inhibition of diamine oxidase (histaminase) causes elevation of histamine levels resulting in headaches, nausea, vomiting, and abdominal pain.[42]

Symptoms

The symptoms of poisoning are typically gastrointestinal and neurological.[29] The symptoms occur within 6-12 hours of consumption, although cases of more severe poisoning may present sooner - as little as 2 hours after ingestion. Initial symptoms are gastrointestinal, with sudden onset of nausea, vomiting, and watery diarrhea which may be bloodstained. Dehydration may develop if the vomiting or diarrhea is severe. Dizziness, lethargy, vertigo, tremor, ataxia, nystagmus, and headaches develop soon after;[29] fever often occurs, a distinctive feature which does not develop after poisoning by other types of mushrooms.[43] In most cases of poisoning, symptoms do not progress from these initial symptoms and patients recover after 2 to 6 days of illness.[28]

In some cases there may be an asymptomatic phase following the initial symptoms which is then followed by more significant toxicity including kidney damage,[44] liver damage, and neurological dysfunction including seizures and coma.[30] These signs usually develop within 1-3 days in serious cases.[29] The patient develops jaundice and the liver and spleen become enlarged, in some cases blood sugar levels will rise (hyperglycemia) and then fall (hypoglycemia) and liver toxicity is seen. Additionally intravascular hemolysis causes destruction of red blood cells resulting in increase in free hemoglobin and hemoglobinuria which can leads to renal toxicity or renal failure. Methemoglobinemia may also occur in some cases. This is where higher than normal levels of methemoglobin, which is a form of hemoglobin that can not carry oxygen, are found in the blood. It causes the patient to become short of breath and cyanotic.[45] Cases of severe poisoning may progress to a terminal neurological phase, with delirium, muscle fasciculations and seizures, and mydriasis progressing to coma, circulatory collapse, and respiratory arrest.[46] Death, if it occurs, is usually after 5 to 7 days.[47]

Treatment

Treatment is mainly supportive; gastric decontamination with activated charcoal may be beneficial if medical attention is sought within a few hours of consumption. However, symptoms take longer than this to develop and patients do not usually present for treatment until many hours after ingestion, thus limiting its effectiveness.[48] If patients have severe vomiting or diarrhea IV fluids can be used to rehydrate the patient.[28] Monitoring of biochemical parameters such as methemoglobin levels, electrolytes, liver and kidney function, urinalysis, and complete blood count is undertaken and any abnormalities are corrected. Dialysis can be used if kidney function is impaired or kidney failing. Hemolysis may require a blood transfusion to replace the lost red blood cells, while methemoglobinemia is treated with intravenous methylene blue.[49]

Pyridoxine, also known as vitamin B6, can be used as an antidote to MMH as MMH inhibits a pyridoxine-dependent step in the synthesis of the neurotransmitter GABA. By giving additional pyridoxine GABA synthesis can continue and symptoms are relieved.[50] Pyridoxine is given at a dose of 25 mg/kg, if symptoms do not improve this can be repeated up to a maximum total daily dose of 15 to 30 g.[51] Pyridoxine does not decrease hepatic toxicity and is only useful for the neurological symptoms.[41][52] Benzodiazepines are given to control seizures, they also modulate GABA receptors and may increase the effect of pyridoxine. Additionally MMH inhibits the chemical transformation of folic acid into its active form, folinic acid, this can be treated by folinic acid given at 20-200 mg daily.[30]

Carcinogenicity

At least 11 different hydrazines have been isolated from Gyromitra esculenta. Many of these hydrazines have been shown to be actively carcinogenic and highly mutagenic in standard assays and produce tumors in experimental animals.[53][54][55][56][57] The toxins may be cumulative[31] and even small amounts may have a carcinogenic effect.[58] It is possible there is a carcinogenic risk for humans who ingest these types of mushrooms.[53] It is not known if the toxins can be completely removed by parboiling.[1]

Consumption

Despite its recognized toxicity, Gyromitra esculenta is marketed and consumed in several countries or states in Europe and North America. It was previously consumed in Germany, with fungi picked in and exported from Poland. Efforts were taken to discourage consumption by prohibiting its sale there once the extent of its toxicity became known.[18] Similarly in Sweden, the Swedish National Food Administration warns it is not fit for human consumption,[59] and restricts purchase of mushrooms to restaurants alone.[60] It is still highly regarded and consumed in Bulgaria, being also sold in markets and picked for export there.[61] In some countries such as Spain, especially in the eastern Pyrenees, they are traditionally considered a delicacy, and many people report consuming them for many years with no ill effects. Despite this, all false morels are listed as hazardous in official mushroom lists published by the Catalan Government in Spain. Selling and purchasing fresh false morels is legal according to Finnish law, where it is also highly regarded.[62] However, the mushrooms are required by law to be accompanied with a warning that they are poisonous and legally prescribed preparation instructions.[63] False morels are also sold prepared and canned, in which case they are ready to be used. As well as Europe, Gyromitra esculenta is consumed in the Great Lakes region and some western states in the United States.[64]

Preparation

To render false morels edible most of the gyromitrin must be removed. The recommended procedure involves either drying and then boiling or boiling the fresh mushroom.[65] To prepare fresh mushroom it is recommended that they are cut into small pieces and boiled twice in copious amounts of water, at least three parts water to one part chopped mushrooms, for at least five minutes, after each boiling the mushroom should be rinsed thoroughly in clean water.[65] Each round of parboiling reduces the gyromitrin contents to a tenth.[66]. The Finnish Wikipedia suggests 6 kg of water for each 1 kg of mushrooms. The gyromitrin will dissolve in the water where it will remain, therefore the parboiling water must be discarded and replaced with fresh water after each boiling. This process is called parboiling, equalling leaching as a unit operation; the gyromitrin is leached off the mushrooms. Drying the mushrooms can also reduce the concentration of gyromitrin; ten days of open air dessication leads to the loss of 90% of gyromitrin.[31] However it is still recommended that the mushroom be boiled after drying.[65]

MMH boils at 87.5 °C (190 °F) and thus readily vaporizes into the air when water containing fresh false morels is boiled.[34] Poorly ventilated spaces allow vapor to accumulate, resulting in gyromitrin poisoning. If boiling the mushrooms indoors, care should be taken to ensure adequate ventilation, and, if symptoms of gyromitrin poisoning appear, immediately seek fresh air.[67]

Even after boiling, small amounts of gyromitrin remain in the mushrooms. Given the possibility of accumulation of toxins, repeated consumption is not recommended.[68]

Prospects for cultivation

Despite its toxicity, Gyromitra esculenta is clearly highly regarded gastronomically by many. Toxin levels corroborate well between mycelium and fruiting bodies, and strains with much lower concentrations of gyromitrin have been discovered. Furthermore, the fungus has been successfully grown to fruiting in culture.[69] Thus there is scope for future research into cultivation of safer strains.[70]

References

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  2. ^ Persoon CH (1800) Comm. Schaeff. Icon. Pict.: 64
  3. ^ Fries EM (1849) Summa veg. Scand., Section Post. (Stockholm):p. 346
  4. ^ Liddell, Henry George and Robert Scott (1980). A Greek-English Lexicon (Abridged edition ed.). Oxford: Oxford University Press. ISBN 0-19-910207-4. {{cite book}}: |edition= has extra text (help)
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  6. ^ North, Pamela (1967). Poisonous Plants and Fungi in colour. Blandford Press & Pharmacological Society of Great Britain. pp. p. 109. OCLC 955264. {{cite book}}: |pages= has extra text (help)
  7. ^ a b c d Arora, David (1986). Mushrooms demystified: a comprehensive guide to the fleshy fungi (2nd ed. ed.). Berkeley: Ten Speed Press. pp. pp. 801-02. ISBN 0-89815-169-4. {{cite book}}: |edition= has extra text (help); |pages= has extra text (help)
  8. ^ a b Lamaison, Jean-Louis (2005). The Great Encyclopedia of Mushrooms. Könemann. pp. p. 230. ISBN 3-8331-1239-5. {{cite book}}: |pages= has extra text (help); Unknown parameter |coauthors= ignored (|author= suggested) (help)
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  15. ^ Benjamin, p. 267
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  58. ^ Benjamin, p. 128-29
  59. ^ Template:Sv iconAndersson, Christer (2007). "Stenmurklan - olämplig att äta". Livsmedelsverket (National Food Administration). Swedish National Food Administration. Retrieved 2008-03-07.
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  64. ^ Simons, DM (1971). "The Mushroom Toxins". Delaware Medical Journal. 43: 177–87.
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  66. ^ Pyysalo H, Niskanen A (1977). "On the occurrence of N-methyl-N-formylhydrazones in fresh and processed false morel, Gyromitra esculenta". J. Agric. Food Chem. 25 (3): 644–7. PMID 558239.
  67. ^ Benjamin, p. 269
  68. ^ Benjamin, p. 278
  69. ^ List PH, Sundermann G (1974). "Achtung! Frühjahrslorcheln". Deutsche Apotheker Zeitung. 114: 331–32.
  70. ^ Benjamin, p. 279

Sources

  • Benjamin, Denis R. (1995). Mushrooms: poisons and panaceas — a handbook for naturalists, mycologists and physicians. New York: WH Freeman and Company. ISBN 0-7167-2600-9.
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