Gyromitra esculenta

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 normally sprouts 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 stipe up to 6 cm (2.4 in) high.

Although potentially fatal if eaten raw, Gyromitra esculenta is a popular delicacy in Scandinavia, Eastern Europe, and the upper Great Lakes region of North America. It may be sold fresh in Finland, but it must be accompanied by warnings and instructions on correct preparation. It is eaten in omelettes, soups, or sautéed in Finnish cuisine. Once popular in the Pyrenees, it is now prohibited from sale for consumption in Spain.

Although it is still commonly consumed after parboiling, recent evidence suggests that even this procedure may not make the fungus entirely safe; thus raising concerns of risk even when prepared properly. When consumed, the false morel's principal active agent, gyromitrin, is metabolized into the toxic compound monomethylhydrazine (MMH). The toxin affects the liver, central nervous system, and sometimes the kidneys. Symptoms of poisoning involve vomiting and diarrhea several hours after consumption, followed by dizziness, lethargy and headache. Severe cases may lead to delirium, coma and death after 5–7 days.

Taxonomy and naming

The fungus was first described by mycologist Christian Hendrik Persoon as Helvella esculenta in 1800, and gained its current accepted binomial name when the Swedish mycologist Elias Magnus Fries placed it in the genus Gyromitra in 1849. The genus name is derived from the Greek terms gyros/γυρος "round" and mitra/μιτρα "headband". Its specific epithet is derived from the Latin esculentus, "edible".

It is known by a variety of common descriptive names such as brain mushroom, turban fungus, elephant ears, or beefsteak mushroom/morel. Dating from the 19th century, the German term lorchel is a result of the older lorche, itself from the 18th century Low German Lorken, aligning with the similar sounding (and similar looking) morchel. The Finnish name Korvasieni is derived from the terms korva "ear", and sieni "mushroom/fungus", while the Swedish Stenmurkla is Sten "stone" and murkla "morel".

Gyromitra esculenta is a member of a group of fungi known as "false morels", named as such for their resemblance to the highly regarded true morels of the genus Morchella. The grouping includes other species of the genus Gyromitra, such as G. infula (elfin saddle), G. caroliniana (beefsteak mushroom) and G. gigas (snow morel). While some of these species contain little to no gyromitrin, many guidebooks 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 eaten by some and considered poisonous by others).

The genus Gyromitra had been classically considered part of the family Helvellaceae, along with the similar-looking elfin saddles of the genus Helvella. Analysis of the ribosomal DNA of many of the Pezizales showed Gyromitra esculenta and the other false morels to be only distantly related to the other members of the Helvellaceae and instead most closely related to the genus Discina, forming a clade which also contains Pseudorhizina and Hydnotrya. Thus the four genera are now included in the family Discinaceae.

Description

Resembling a brain, 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 grows and ages. The cap colour may be various shades of reddish-, chestnut-, purplish-, bay-, dark or sometimes golden-brown. Specimens from California may have more reddish-brown caps. Attached to the cap at several points, the stipe is 3–6 cm (1.2–2.4 in) high and 2–3 cm (0.8–1.2 in) wide. Gyromitra esculenta has a solid stipe whereas those of true morels (Morchella spp.) are hollow. 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 that are elliptical and 17–22 μm in length.

G. esculenta resembles the various species of true morel, although the latter are more symmetric and look more like pitted gray, tan, or brown sponges. Its cap is generally darker and larger.

Distribution and habitat

Gyromitra esculenta grows on sandy soil in coniferous and occasionally deciduous woodlands. Among conifers it is mostly found under pines (Pinus spp.), but also sometimes aspen (Populus spp.). The hunting period is from April to July, earlier than for other species, and the fungus may even sprout up with the melting snow. It can be abundant 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. Enthusiasts in Finland have been reported burying newspaper inoculated with the fungus in the ground in autumn and returning the following spring to collect mushrooms.

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, as far south as Mexico. It is also common in Central Europe, less abundant in the east, and more in montane areas than lowlands. It has been recorded from Northern Ireland, from Uşak Province in Western Turkey, and from the vicinity of Kaş in the Antalya Province of Turkey's southern coast.

Toxicity

Toxic reactions have been known for at least a hundred years. Experts speculated the reaction was more of an allergic one related to the consumer, or misidentification, rather than innate toxicity of the fungus, due to the wide range in effects seen. 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 Gyromitra esculenta for many years without ill-effects. However, the fungus is now widely recognized as potentially deadly.

Gyromitra esculenta contains the poison 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. A 1971 Polish study reported at the time that the species accounted for up to 23% of mushroom fatalities each year. Death rates have dropped since the mid-twentieth century; 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.

A lethal dose of gyromitrin has been estimated to be 10–30 mg/kg for children and 20–50 mg/kg in adults. These doses correspond to around 0.2–0.6 kg (6 oz.–1lb. 5oz. and 0.4–1 kg (13 oz.–2 lb. 3 oz. ) of fresh mushroom respectively. However, individual responses may vary and people who have ingested similar amounts may develop anything from minimal to severe toxicity. Evidence suggests 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. Although the amount of gyromitrin present can be significantly reduced through parboiling (leaching), it is a cumulative poison, and there is evidence that repeated consumption can increase risk of toxicity.

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, and there is some evidence that fungi west of the Rocky Mountains in North America contain less toxin than those to the east. However, poisonings in the west have been reported, although they have been reported less frequently than the east.

Biochemistry

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

The toxins react with pyridoxal-5-phosphate—the activated form of pyridoxine—and form a hydrazone. This reduces production of the neurotransmitter GABA via decreased activity of glutamic acid decarboxylase, producing the neurological symptoms. MMH also causes oxidative stress leading to methemoglobinemia. Additionally during the metabolism of MMH, N-methyl-N-formylhydrazine is produced; this then undergoes cytochrome p450 regulated oxidative metabolism which via reactive nitrosamide intermediates leads to formation of methyl radicals which lead to liver necrosis. Inhibition of diamine oxidase (histaminase) elevates histamine levels resulting in headaches, nausea, vomiting, and abdominal pain.

Symptoms

The symptoms of poisoning are typically gastrointestinal and neurological. 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; fever often occurs, a distinctive feature which does not develop after poisoning by other types of mushrooms. In most cases of poisoning, symptoms do not progress from these initial symptoms and patients recover after 2–6 days of illness.

In some cases there may be an asymptomatic phase following the initial symptoms which is then followed by more significant toxicity including kidney damage, liver damage, and neurological dysfunction including seizures and coma. These signs usually develop within 1–3 days in serious cases. 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. 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. Death may occur from five to seven days after consumption.

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 often take longer than this to develop and patients do not usually present for treatment until many hours after ingestion, thus limiting its effectiveness. Patients with severe vomiting or diarrhea can be rehydrated with intravenous fluids. 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 the kidneys are failing. Hemolysis may require a blood transfusion to replace the lost red blood cells, while methemoglobinemia is treated with intravenous methylene blue.

Also known as vitamin B6, pyridoxine can be used to counteract the inhibition by MMH on the pyridoxine-dependent step in the synthesis of the neurotransmitter GABA. Thus GABA synthesis can continue and symptoms are relieved. Pyridoxine, which is only useful for the neurological symptoms and does not decrease hepatic toxicity, is given at a dose of 25 mg/kg; this can be repeated up to a maximum total of 15 to 30 g daily if symptoms do not improve. Benzodiazepines are given to control seizures, as they 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.

Carcinogenicity

At least 11 different hydrazines have been isolated from Gyromitra esculenta. Many of these have been shown to be actively carcinogenic and highly mutagenic in standard assays and produce tumors in experimental animals. The toxins may be cumulative and even small amounts may have a carcinogenic effect. Although Gyromitra esculenta has not been observed to cause cancer in humans, it is possible there is a carcinogenic risk for people who ingest these types of mushrooms. It is not known if the potential carcinogens can be completely removed by parboiling.

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. Once the extent of its toxicity became known, Germany and Switzerland discouraged consumption by prohibiting its sale. Similarly in Sweden, the Swedish National Food Administration warns it is not fit for human consumption, and restricts purchase of mushrooms to restaurants alone. The mushroom is still highly regarded and consumed in Bulgaria, being sold in markets and picked for export there. 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, the false morel is listed as hazardous in official mushroom lists published by the Catalan Government in Spain and sale for consumption is prohibited. Selling and purchasing fresh false morels is legal according to Finnish law, where it is highly regarded. However, the mushrooms are required by law to be accompanied with a warning that they are poisonous and legally prescribed preparation instructions. False morels are also sold prepared and canned, in which case they are ready to be used. Official figures from the Finnish Ministry of Agriculture and Forestry report a total amount of false morels sold in Finland of 21.9 tonnes in 2006 and 32.7 tonnes, noted as being above average, in 2007. In 2002, the Finnish Food Safety Authority estimated annual consumption of false morels to be hundreds of tonnes in plentiful years. Outside of Europe, Gyromitra esculenta is consumed in the Great Lakes region and some western states in the United States.

In Finnish Cuisine, false morels may be cooked in an omelette, or gently sautéed in butter in a saucepan, flour and milk added to make a bechamel sauce, or pie filling. Alternately, more fluid can be added for a false morel soup. Typical condiments added for flavour include parsley, chives, dill and black pepper.

Preparation

Most of the gyromitrin must be removed to render false morels edible. The recommended procedure involves either first drying and then boiling the mushrooms, or boiling the fresh mushrooms directly. 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. Each round of parboiling reduces the gyromitrin contents to a tenth. The gyromitrin is leached into the water where it will remain, therefore the parboiling water must be discarded and replaced with fresh water after each round of boiling. Drying the mushrooms can also reduce the concentration of gyromitrin; ten days of open air desiccation leads to the loss of 90% of gyromitrin. However it is still recommended that the mushroom be boiled after drying.

MMH boils at and thus readily vaporizes into the air when water containing fresh false morels is boiled. 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. Even after boiling, small amounts of gyromitrin remain in the mushrooms. Given the possibility of accumulation of toxins, repeated consumption is not recommended.

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. Thus there is scope for future research into cultivation of safer strains.

References

General

Benjamin, Denis R. (1995). Mushrooms: poisons and panaceas — a handbook for naturalists, mycologists and physicians. New York: WH Freeman and Company. Specific