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Amanita phalloides

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Death cap
Secure
Scientific classification
Kingdom:
Fungi
Division:
Basidiomycota
Class:
Homobasidiomycetes
Subclass:
Hymenomycetes
Order:
Agaricales
Family:
Amanitaceae
Genus:
Amanita
Species:
A. phalloides
Binomial name
Amanita phalloides
Amanita phalloides
View the Mycomorphbox template that generates the following list
Gills on hymenium
Cap is convex or flat
Hymenium is free
Stipe has a ring and volva
Spore print is white
Ecology is mycorrhizal
Edibility is deadly

Amanita phalloides, commonly known as the death cap, is a poisonous basidiomycete fungus, one of many in the genus Amanita. Widely distributed across Europe, A. phalloides associates with various deciduous and coniferous trees. Adaptations have expanded its range outside Europe after it was accidentally introduced alongside oak, chestnut, and pine. The large fruiting bodies (i.e., the mushrooms) appear in summer and autumn; the caps are generally greenish in colour, with a white stipe and gills.

Coincidentally, these toxic mushrooms resemble several edible species commonly consumed by humans, increasing the risk of accidental poisoning. A. phalloides is one of the most poisonous of all known toadstools. It has been involved in the majority of human deaths from mushroom poisoning, including possibly the deaths of Roman Emperor Claudius and Holy Roman Emperor Charles VI. It has been the subject of much research, and many of its biologically active agents have been isolated. The principal toxic constituent is α-amanitin, which damages the liver and kidneys, often fatally. No antidote is known.

Taxonomy and naming

The death cap was first described by French botanist Sébastien Vaillant in 1727, who gave a succinct phrase name "Fungus phalloides, annulatus, sordide virescens, et patulus", which is still recognizable as the fungus today.[1] Though the scientific name phalloides means "phallus-shaped", it is unclear whether it is named for its resemblance to a literal phallus or the stinkhorn mushrooms Phallus. In 1821, Elias Magnus Fries described it as Agaricus phalloides, but included all white Amanitas within its description.[2] Finally in 1833, Johann Heinrich Friedrich Link settled on the name Amanita phalloides,[3] after Persoon had named it Amanita viridis thirty years earlier.[4][5] Although Louis Secretan's use of the name Amanita phalloides predates Link's, it has been rejected for nomenclatural purposes because Secretan's works did not use binomial nomenclature consistently;[6][7] some taxonomists have, however, disagreed with this opinion.[8][9]

Amanita phalloides is the type species of Amanita section Phalloideae, a group that contains all of the deadly poisonous Amanita species thus far identified. Most notable of these are the species known as destroying angels, namely Amanita virosa and A. bisporiga as well as the fool's mushroom (A. verna). The term "destroying angel" has been applied to A. phalloides at times, but "death cap" is by far the most common vernacular name used in English. Other common names also listed include "stinking amanita"[10] and "deadly amanita".[11]

A rarely appearing all-white form was initially described A. phalloides f. alba by Max Britzelmayr,[12][13] though its status has been unclear. It is often found growing amid normally coloured death caps. It has been described, in 2004, as a distinct variety and includes what was termed A. verna var. tarda.[14] The true Amanita verna fruits in spring and turns yellow with KOH solution, whereas A. phalloides never does.[15]

Description

Appearing after periods of precipitation from late summer through autumn,[16] the death cap has a large and imposing epigeous (aboveground) fruiting body (basidiocarp), usually with a pileus (cap) from 5 to 15 cm (2–6 in) across, initially rounded and hemispherical, but flattening with age.[17] The colour of the cap can be pale-, yellowish-, or olive-green, often paler toward the margins and often paler after rain. The cap surface is sticky when wet and easily peeled, a troublesome feature, as that is allegedly a feature of edible fungi.[18] The remains of the partial veil is seen as a skirtlike, floppy annulus usually about 1 to 1.5 cm (0.4–0.6 in) below the cap. The crowded white lamellae (gills) are free. The stipe is white with a scattering of grayish-olive scales and is 8 to 15 cm (3–6 in) long and 1 to 2 cm (3/8–3/4 in) thick, with a swollen, ragged, sac-like white volva (base).[17] As the volva, which may be hidden by leaf litter, is a distinctive and diagnostic feature, it is important to remove some debris to check for it.[19]

The smell has been described as initially faint and honey-sweet but strengthening over time to become overpowering, sickly-sweet and objectionable.[16] Young specimens first emerge from the ground resembling a white egg covered by a universal veil, which then breaks, leaving the volva as a remnant. The spore print is white, a common feature of Amanita. The transparent spores are globular to egg-shaped, measure 8–10 μm (0.3–0.4 mil) long, and stain blue with iodine.[16] The gills, on the other hand, are seen to stain pallid lilac or pink with concentrated sulfuric acid.[20][21]

A young death cap emerging from universal veil (France)

Distribution and habitat

The death cap is native to Europe, where it is widespread.[22] It is found from the southern coastal regions of Scandinavia in the north, to Ireland in the west, east to Poland and western Russia,[14] and south throughout the Balkans, in Italy and Spain, and in Morocco and Algeria in north Africa.[23] There are records from further east into Asia but these have yet to be confirmed as A. phalloides.[24]

It is ectomycorrhizally associated with a number of tree species. In Europe, these include a large number of hardwood and, less frequently, conifer species. It appears most commonly under oaks but also under beeches, chestnuts, horse-chestnuts, birches, filberts, hornbeams, pines, and spruces.[12] In other areas, A. phalloides may also be associated with these trees or only with some species but not others. In coastal California, for example, A. phalloides is associated with coast live oak but not with the various coastal pine species, such as Monterey pine.[25] In countries where it has been introduced it has been restricted to those exotic trees it would associate with in its natural range. There is, however, evidence of A. phalloides associating with hemlock and with genera of the Myrtaceae: Eucalyptus in Tanzania[26] and Algeria,[23] and Leptospermum and Kunzea in New Zealand.[27][12] This suggests the species may have invasive potential.[24]

By the end of the 19th century, Charles Horton Peck had reported A. phalloides in North America.[28] However, in 1918, samples from the Eastern United States were identified as being a distinct though similar species, A. brunnescens, by G. F. Atkinson of Cornell University.[29] By the 1970s it had become clear that A. phalloides actually does occur in the United States, apparently having been introduced from Europe alongside chestnuts, with populations on the West and East Coasts.[29][30] A more recent historical review concluded that the East Coast populations were introduced but that the origins of the West Coast population remain unclear, due to the scantness of historical records.[24]

Amanita phalloides has been conveyed to new countries across the southern hemisphere with the importation of hardwoods and conifers. Introduced oaks appear to have been the vector to Australia and South America; populations under oaks have been recorded from Melbourne and Canberra,[31][32] as well as Uruguay.[33] It has been recorded under other introduced trees in Argentina[34] and Chile.[35] Pine plantations are associated with the fungus in Tanzania[26] and South Africa, where it is also found under oaks and poplars.[36]

Toxicity

Warning sign in Canberra, Australia

As the common name suggests, the fungus is highly toxic, and it is responsible for the majority of fatal mushroom poisonings worldwide.[37] It is estimated that 30 grams (1 oz), or half a cap, of this mushroom is enough to kill a human.[38] In 2006, a family of three in Poland was poisoned, resulting in one death and the two survivors requiring liver transplants.[39] Some authorities strongly advise against putting suspected death caps in the same basket with fungi collected for the table and to avoid touching them.[18][40] Furthermore, the toxicity is not reduced by cooking, freezing, or drying. Its biochemistry has been researched intensively for decades.[29]

Similarity to edible species

Recent cases highlight the issue of the similarity of A. phalloides to the edible paddy straw mushroom, Volvariella volvacea, with east- and southeast-Asian immigrants in Australia and the west coast of the United States falling victim. In an episode in Oregon, four members of a Korean family required liver transplants.[41] Of the seven people poisoned in the Canberra region between 1988 and 1998, three were from Laos.[42] This misidentification is a leading cause of mushroom poisoning in the United States.

Novices may mistake juvenile death caps for edible puffballs[43] or mature specimens for other edible Amanita species such as Amanita lanei, and for this reason some authorities recommend avoiding the collecting of Amanita species for the table altogether.[44] The white form of A. phalloides may be mistaken for edible species of Agaricus, especially the young fruitbodies whose unexpanded caps conceal the telltale white gills; all mature species of Agaricus have dark-coloured gills.[45]

In Europe, other similarly green-capped species collected by mushroom hunters include various green-hued brittlegills of the genus Russula and the formerly popular Tricholoma flavovirens, now regarded as hazardous owing to a series of restaurant poisonings in France. Brittlegills, such as Russula heterophylla, R. aeruginea, and R. virescens, can be distinguished by their brittle flesh and the lack of both volva and ring.[46] Other similar species include A. subjunquillea in eastern Asia and A. arocheae, which ranges from Andean Colombia north at least as far as central Mexico, both of which are also poisonous.

Biochemistry

The species is now known to contain two main groups of toxins, both multicyclic (ring-shaped) peptides, spread throughout the mushroom tissue: the amatoxins and the phallotoxins. Another toxin is phallolysin, which has shown some hemolytic (red blood cell–destroying) activity in vitro. An unrelated compound, antamanide, has also been isolated.

Amatoxins consist of at least eight compounds with a similar structure, that of eight amino-acid rings; they were isolated in 1941 by Heinrich O. Wieland and Rudolf Hallermayer of the University of Munich.[29] Of the amatoxins, α-amanitin is the chief component and along with β-amanitin is likely responsible for the toxic effects.[47][48] Their major toxic mechanism is the inhibition of RNA polymerase II, a vital enzyme in the synthesis of messenger RNA (mRNA), microRNA, and small nuclear RNA (snRNA). Without mRNA essential protein synthesis and hence cell metabolism grind to a halt and the cell dies.[49] The liver is the principal organ affected, as it is the organ which is first encountered after absorption in the gastrointestinal tract, though other organs, especially the kidneys, are susceptible.[50]

The phallotoxins consist of at least seven compounds, all of which have seven similar peptide rings. Phalloidin was isolated in 1937 by Feodor Lynen, Heinrich Wieland's student and son-in-law, and Ulrich Wieland of the University of Munich. Though phallotoxins are highly toxic to liver cells,[51] they have since been found to have little input into the death cap's toxicity as they are not absorbed through the gut.[49] Furthermore, phalloidin is also found in the edible (and sought-after) Blusher (Amanita rubescens).[29] Another group of minor active peptides are the virotoxins, which consist of six similar monocyclic heptapeptides.[52] Like the phallotoxins they do not exert any acute toxicity after ingestion in humans.[49]

Symptoms

Death caps have been reported to taste pleasant.[29][53] This, coupled with the delay in the appearance of symptoms—during which time internal organs are being severely, sometimes irreparably, damaged—makes it particularly dangerous. Initially, symptoms are gastrointestinal in nature and include colicky abdominal pain, with watery diarrhea and vomiting which may lead to dehydration, and, in severe cases, hypotension, tachycardia, hypoglycemia, and acid-base disturbances.[54][55] These first symptoms resolve two to three days after the ingestion. A more serious deterioration signifying liver involvement may then occur—jaundice, diarrhea, delirium, seizures, and coma due to fulminant hepatic failure and attendant hepatic encephalopathy caused by the accumulation of normally liver-removed substance in the blood.[10] Renal failure (either secondary to severe hepatitis[56][52] or caused by direct toxic renal damage[49]) and coagulopathy may appear during this stage. Life-threatening complications include increased intracranial pressure, intracranial hemorrhage, sepsis, pancreatitis, acute renal failure, and cardiac arrest.[54][55] Death generally occurs six to sixteen days after the poisoning.[57]

Up to the mid-20th century, the mortality rate was around 60–70%, but this has greatly improved with advances in medical care. A review of death cap poisoning throughout Europe from 1971 to 1980 found the overall mortality rate to be 22.4% (51.3% in children under ten and 16.5% in those older than ten).[58] This has fallen further in more recent surveys to around 10–15%.[59]

Treatment

Consumption of the death cap is a medical emergency requiring hospitalization. There are four main categories of therapy for poisoning: preliminary medical care, supportive measures, specific treatments, and liver transplantation.[60]

Preliminary care consists of gastric decontamination with either activated carbon or gastric lavage. However, due to the delay between ingestion and the first symptoms of poisoning, it is commonplace for patients to arrive for treatment many hours after ingestion, potentially reducing the efficacy of these interventions.[60][61] Supportive measures are directed towards treating the dehydration which results from fluid loss during the gastrointestinal phase of intoxication and correction of metabolic acidosis, hypoglycemia, electrolyte imbalances, and impaired coagulation.[60]

No definitive antidote is available, but some specific treatments have been shown to improve survivability. High-dose continuous intravenous penicillin G has been reported to be of benefit, though the exact mechanism is unknown,[58] and trials with cephalosporins show promise.[62][63] There is some evidence that intravenous silibinin, an extract from the blessed milk thistle (Silybum marianum), may be beneficial in reducing the effects of death cap poisoning. Silibinin prevents the uptake of amatoxins by hepatocytes, thereby protecting undamaged hepatic tissue; it also stimulates DNA-dependent RNA polymerases, leading to an increase in RNA synthesis.[64][65][66] N-acetylcysteine has shown promise in combination with other therapies.[67] Animal studies indicate the amatoxins deplete hepatic glutathione;[68] N-acetylcysteine serves as a glutathione precursor and may therefore prevent reduced glutathione levels and subsequent liver damage.[69] None of the antidotes used have undergone prospective, randomized clinical trials, and only anecdotal support is available. Silibinin and N-acetylcysteine appear to be the therapies with the most potential benefit.[60] Repeated doses of activated carbon may be helpful by absorbing any toxins that are returned to the gastrointestinal tract following enterohepatic circulation.[70] Other methods of enhancing the elimination of the toxins have been trialed; techniques such as hemodialysis,[71] hemoperfusion,[72] plasmapheresis,[73] and peritoneal dialysis[74] have occasionally yielded success but overall do not appear to improve outcome.[49]

In patients developing liver failure, a liver transplant is often the only option to prevent death. Liver transplants have become a well-established option in amatoxin poisoning.[55][54][75] This is a complicated issue, however, as transplants themselves may have significant complications and mortality; patients require long-term immunosuppression to maintain the transplant.[60] That being the case, there has been a reassessment of criteria such as onset of symptoms, prothrombin time (PTT), serum bilirubin, and presence of encephalopathy for determining at what point a transplant becomes necessary for survival.[76][77][78] Evidence suggests that, although survival rates have improved with modern medical treatment, in patients with moderate to severe poisoning up to half of those who did recover suffered permanent liver damage.[79] However, a follow-up study has shown that most survivors recover completely without any sequelae if treated within 36 hours of mushroom ingestion.[80]

Notable victims

Several historical figures may have died from Amanita phalloides poisoning (or other similar, toxic Amanitas). These were either accidental poisonings or assassination plots. Alleged victims of this kind of poisoning include Roman Emperor Claudius, Pope Clement VII, Tsaritsa Natalia Naryshkina, and Holy Roman Emperor Charles VI.[81]

R. Gordon Wasson recounted the details of these deaths, noting the likelihood of Amanita poisoning. In the case of Clement VII, the illness that led to his death lasted some five months, making the case clearly inconsistent with amatoxin poisoning. Natalia Naryshkina is said to have consumed a large quantity of pickled mushrooms prior to her death. However, it is unclear whether the mushrooms themselves were poisonous or whether she succumbed to food poisoning.[81]

Ce plat de champignons a changé la destinée de l’Europe.

("This dish of mushrooms changed the destiny of Europe.")

— Voltaire, Mémoires.

Charles VI experienced indigestion after eating a dish of sautéed mushrooms. This led to an illness from which he died ten days later — symptomology consistent with amatoxin poisoning. Charles' death led to the War of Austrian Succession. Noted Voltaire, "this dish of mushrooms changed the destiny of Europe."[82][81]

The case of the Claudius poisoning is more complex. It is known that Claudius was very fond of eating Caesar's mushroom. Following his death, many sources have attributed it to his being fed a meal of death caps instead of Caesar's mushrooms. However, ancient authors such as Tacitus and Suetonius are unanimous about there having been poison added to the mushroom dish, rather than the dish having been prepared from poisonous mushrooms. Wasson speculates that the poison used to kill Claudius was derived from death caps, with a fatal dose of colocynth being administered later during his illness.[83][81]

Footnotes

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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.
  • Jordan Peter, Wheeler Steven. (2001). The Ultimate Mushroom Book. London: Hermes House. ISBN 1-85967-092-X.
  • Zeitlmayr, Linus (1976). Wild Mushrooms:An Illustrated Handbook. Hertfordshire: Garden City Press. ISBN 0-584-10324-7.
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