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Home , Amanita pantherina, Strychnine

Case report — Gevalverslag

Suspected poisoning of puppies by the pantherina

T W Naudéa and W L Berryb

encountered, and therefore seldom ABSTRACT recorded. A serious complicating factor in Amanita pantherina poisoning is suspected as the cause of a severe, transient neurological the diagnosis of mushroom intoxication disorder in three 5-week-old German shepherd puppies. There was very strong circum- in animals is their inability to communi- stantial evidence that this mushroom had been eaten, and the signs encountered were cate that have been ingested. similar to those described in confirmed field cases of intoxication in dogs. It was also in Furthermore, the soft texture of the fungi many respects consistent with the syndrome seen in humans. A veterinary perspective on results in rapid fragmentation, so that the hallucinogenic Amanita spp. is given and the veterinary literature on mushroom they may not be readily recognised in intoxication is briefly reviewed as, in contrast to humans, it is not often reported in animals. This is the 1st report of suspected mushroom intoxication of animals in South Africa. vomitus, lavage fluid or at necropsy. In addition, there are the problems of Key words: Amanita pantherina, canine, coma, , , syndrome divergence (vide supra) and the intoxication, . lack of knowledge required to identify the Naudé T W, Berry W L Suspected intoxication of puppies by the mushroom Amanita causative mushroom and connect it pantherina. Journal of the South African Veterinary Association (1997) 68(4): 154–158 (En.). with the signs of intoxication observed. Department of Pharmacology and Toxicology, Faculty of Veterinary Science, University of Nevertheless, a number of mushroom Pretoria, Private Bag X04, Onderstepoort, 0110 South Africa. intoxications have been reported in the veterinary literature that correspond more or less with the above syndrome INTRODUCTION methylhydrazine and causing similar classification for humans18. Mushrooms are divided into those that but less severe cytotoxicity. This report describes the 1st recorded are edible, those that are not edible and 4. A group causing -related case of suspected Amanita pantherina those that are definitely toxic. The last symptoms such as salivation and poisoning in dogs in South Africa, with a group are popularly referred to as toad- increased gastrointestinal motility. brief review of the veterinary literature on stools, a name anglicised from the 5. An interesting group that causes . German ‘todestuhl’ (death chair), sensitivity to by inhibition of apparently derived from the belief that acetaldehyde dehydrogenase (thus MUSHROOM POISONING IN toads sitting on these fungi render them not of veterinary importance). ANIMALS toxic (McKenney and Stutz cited by 6. The hallucinogenic mushrooms. This A review of the veterinary literature Ridgway27). From a clinical and diagnostic category can be subdivided into the according to species revealed the follow- perspective in humans, toxic mushrooms -group, causing an halluci- ing: are grouped by Lampe18 according to the genic syndrome not associated with Mushroom intoxication is rare in 6 main syndromes encountered: sleep or coma, and a group causing ruminants. Ramaria flavo-brunnescens is the 1. A diverse group responsible for delirium associated with sleep or only mushroom known to regularly usually transient gastrointestinal coma. Both Amanita pantherina and cause intoxication in cattle and sheep in irritation ascribed to a variety of A. muscaria fall into the latter group. Brazil and Paraguay. The syndrome was (probably the most commonly seen Ramaria flavo-brunnescens poisoning of recently reproduced again in cattle syndrome). ruminants constitutes a exceptional addi- and the pathology described in detail. It 2. The Amanita phalloides-group, contain- tional clinical veterinary category, in appears that the results in no or ing cyclic polypeptides responsible for which the toxin interferes with keratinisa- incomplete and irregular keratinisation the most serious and often fatal tion17. of keratinocytes, leading to loss of intoxication: delayed, irreversible Mushroom poisoning in humans is hooves, horns, tail hair and smoothing cytotoxicity affecting predominantly relatively common and is well recorded. of the dorsum of the tongue17. This the liver and kidney. The most important factors contributing unique intoxication syndrome is, to our 3. The Gyrometra-group, containing to intoxication are, firstly, confusion of knowledge, the only mushroom toxic mushrooms with edible species, as poisoning that has not been recorded in considerable experience is required to humans. This mushroom is associated differentiate between them, and secondly with Eucalyptus trees and the poisoning is, aEmiritus Professor, Department of Pharmacology and Toxicology, Faculty of Veterinary Science, University of the recently emerging but widespread therefore, commonly known as Eucalyptus Pretoria. Present address: Division of Toxicology, practice of deliberate use of hallucino- disease. Neither the syndrome nor the Onderstepoort Veterinary Institute, Private Bag X05, Onderstepoort, 0110 South Africa. genic mushrooms for ‘recreational species has been recorded in this region, 23 bDepartment of Medicine, Faculty of Veterinary Science, purposes’ . although a related species, R. formosa, University of Pretoria. Present address: Neurol- Except for Ramaria17, animals apparently occurs in the Western Cape Province in ogy/Neurosurgery Service, Veterinary Medical Teaching Hospital, School of Veterinary Medicine, University of do not eat mushrooms by choice to any association with bluegum (Eucalyptus) California, Davis, CA 95616, USA. extent. Consequently, intoxication is trees and ingestion is reported to 30 Received: September 1997. Accepted: November 1997. incidental, apparently not frequently result in severe diarrhoea in humans . In

154 0038-2809 Tydskr.S.Afr.vet.Ver. (1997) 68(4): 154–158 sheep in northern Europe, Cortinarius specimen of the same species died. No vestibular signs and convulsions followed speciosissimus proved to be the cause of pathological data were, however, by coma. When occurred fatal kidney damage24. The genus occurs recorded9. Only 1 case where a 7-week- 9 h later, artificial respiration was applied locally in South Africa19 but is apparently old pup was seen eating botanically for 45 min., but normal breathing only not common. Only 2 further speculative identified A. verna a day before death resumed after intravenous corticosteroid case reports could be traced, describing is recorded. The pathology and histo- therapy. The coma, however, lasted for a gastroenteritis in cattle that might have pathology in this case, as well as in a 12- further 5 h and was followed by unevent- resulted from ingestion of mushrooms7,25. week-old pup where the mushroom that ful recovery21. Probably because horses are fastidious was eaten was not available but the owner grazers, only 1 report, describing described something resembling A. phal- CASE REPORT suspected hallucinogen-containing loides, were consistent with this category mushroom intoxication13, could be found. of intoxication20. In a confirmed case of History Similarly, despite the fact that swine are Category 3 intoxication (less severe The incident occurred in January 1991 omnivorous, only a single case of intoxica- hepatotoxicity), a 10-week-old cocker on a small agricultural holding just east of tion in a Chinese pot-bellied miniature spaniel was observed eating a mushroom, Pretoria where the owner had been living pig, ascribed to ingestion of Scleroderma vomited 2–3 h later, became lethargic for 18 years. A number of well-established citrinum, has been recorded11. This after 6 h and was presented comatose to trees occur on the property, including common earth ball (or puff ball) is widely the veterinarian. It died 30 min later. a number of Cedrus deodora (deodar distributed in the more humid parts of Pathological investigation revealed indi- cedars). A German shepherd bitch with southern Africa, where it is associated cations of a haemolytic crisis with renal six 51⁄2-week-old pups was kept in a well- with pine trees30. tubular necrosis and periacinar hepatic constructed, lock-up kennel with a Cats also apparently do not eat mush- degeneration, leucocytosis and erythro- cement floor. During the day the bitch rooms to any extent, as only 1 article phagocytosis. Samples collected in the roamed freely and the pups had access to describing 2 incidents of suspected mush- pasture where the dog was found a kikuyu lawn extension in front of the room intoxication in this species could be chewing the mushroom proved to be kennel that was temporarily enclosed traced22. In 1 case, transient gastrointesti- Gyrometra esculenta which contains with loose partitions of coarse mesh wire nal irritation and near coma occurred in a monomethylhydrazine1. This genus has fencing. This fence had contained the cat that had been eating an unidentified not been recorded in South Africa pups successfully up to that stage, but as mushroom. In the other case, neurological (A Eicker, Department of Botany, Univer- they became older and stronger they signs and neuropathology in addition to sity of Pretoria, pers. comm., 1997). started to crawl through the loose fencing liver necrosis of undetermined origin Transient and diarrhoea and roam nearby. were attributed to possible mushroom occurred in a 14-year-old springer spaniel At 06:00 on the morning of the incident intoxication. after it had eaten 4 mushroom species, of the owner found a male pup apparently The dog is the only species that appears which the dominant one identified in the stuck in the fence. When it was released to be affected relatively frequently by vomitus was the known toxic she observed that its ‘neck flopped back’. toxic mushrooms, with 9 traceable reports phaeocromis32. This mushroom belongs to It appeared weak, disorientated and un- of intoxication involving 20 41⁄2–12-weeks- the muscarine-containing Category 4 able to walk. Neck injury was suspected old pups and 9 adult individuals. (vide supra) and is represented locally by and the pup was admitted to a private A case of suspected Category 1 mush- I. eutheles, which occurs in the southern practice. By 09:00 a 2nd pup (also male) room intoxication (gastrointestinal irrita- Western Cape Province30. was found paralysed. Its head was also tion) involved a litter of five 7-week-old Concerning hallucinogenic mushroom thrown back, the jaws were clamped, the boxers that developed black tarry intoxication in the dog, confirmed cases in eyes rolled and it could not rise. This pup diarrhoea. The faeces contained no blood, both the above Category 6 intoxication also was taken to the veterinarian, who and flotation and direct smears of the syndromes (with and without coma) are referred both cases to the Veterinary faeces revealed numerous mushroom recorded: Academic Hospital of the Faculty of spores that unfortunately could not be An adult Labrador showing ataxia, Veterinary Science at Onderstepoort further identified. Symptomatic treat- , vocalisation and overt aggres- (OVAH). At 20:00 on the same day, the ment resulted in uneventful recovery31. sion without subsequent coma had to be owner reported that a 3rd pup developed Despite many cases of fatal hepato- and given sedation. Subsequently, similar (but less pronounced) signs. nephrotoxicity (Category 2 poisoning) in psillocybin was chemically demonstrated According to the owner, it was very humans (also in South Africa) by the in its blood16. lethargic and dull, and although it slept in highly toxic cyclopeptide-containing In the category of hallucination with an apparent coma, it was ‘jerky’ to tactile Amanita spp., most of the literature deals concomitant coma, 1 confirmed case in and auditory stimuli. This pup appeared with experimental intoxication in dogs10. Canada12 and 1 case of suspected poison- normal the following morning, and was Only 3 reports of field intoxication in ing in the United States of America21 are not examined by a veterinarian. It passed dogs were traced: 6 fatal cases occurred in reported. In the former case, Amanita soft slimy faeces during the night that were the United States of America, in which pantherina ingestion by a litter of 9 collected for laboratory examination. the typical histopathological lesions 41⁄2-week-old Labradors resulted in severe supported the diagnosis. In 3 of these paresis and in 5 pups, 3 of Clinical and laboratory evaluation cases, chewed A. phalloides was collected which died within 3 h of ingestion. and treatment on the property and botanically identi- Convulsions were encountered for 12 h in One male pup was presented in lateral fied, and in the other 3 cases ingestion was the other 2, but they had recovered com- recumbency and semi-comatose, with suspected15. In Australia, a 9-week-old pletely 17 h later12. Suspected Amanita opisthotonus, right lateral strabismus, spaniel pup that had consumed a small muscaria poisoning in a 4-year-old male paddling and exhibited chewing move- portion of a cap of a botanically identified collie resulted in apparent confusion, ments. The other dog was quadriparetic

0038-2809 Jl S.Afr.vet.Ass. (1997) 68(4): 154–158 155 and depressed, with left lateral strabis- mus. Both dogs had severely miotic pupils, congested mucous membranes, raised rectal temperatures (39.9 and 39.5 °C), pulse rates >150/min and were panting. A preliminary diagnosis of possi- ble intoxication was made, and the dogs were sedated with (Valium, Roche) at 0.5 mg/kg intravenously. One of the pups subsequently developed cardio- respiratory arrest. Intubation, positive pressure ventilation, and cardiac massage were successful in resuscitating the pup. was performed on this pup during the immediate post-resuscitation period while the endotracheal tube was still in place. Consciousness returned after 5 min. Blood samples were collected in EDTA, heparin, sodium fluoride and plain test tubes for haematology, serum chemistry and toxicological investigation. The gastric content was submitted for strychnine determination. Fig. 1: Amanita pantherina (photograph: A Eicker). Polyionic fluid (Plasmalyte B, Sabax) was administered to both puppies via jugular catheters, and (1 mg/kg) The mushrooms were recognised imme- It has a diameter of 6–10 cm and the gills administered, half intravenously and half diately as A. pantherina, and the identity (lamellae) are white. The white cylindrical subcutaneously. Within 4 h the 2 dogs subsequently confirmed by the Botany to clavate stem (or ) of up to 10 cm were ambulatory and appeared clinically Department of the University of Pretoria. high and 1.0–1.5 cm wide often thickens normal. An in loco inspection the same evening to a bulbous base of 2.5–3.0 cm and is An inflammatory leukogram was pre- revealed that a young deodar cedar, surmounted by a free-standing cup, rim sent in 1 dog and both were mildly hyper- with the lowest branches almost touching or collar of volval tissue just below soil glycaemic (12.8 and 6.9 mmol /l). the ground, was growing adjacent to the surface. A clearly-defined persistent ring Normal blood acetylcholinesterase temporary fence around the pups’ (the annulus) with a double margin activity ruled out organophosphor kikuyu-lawn run. The low branches and occurs around the stem just below the , and the stomach content was mass of fine needles under the tree cap19,26. Like most Amanita spp., the negative for strychnine. Faecal smears of created an undisturbed area where mycelium of this mushroom interacts the 2 pups revealed small, darkly stained several of these mushrooms’ fruiting symbiotically with the hair roots of a objects suggestive of fungal spores. bodies were found. One particular particular host tree in a mycorrhizal However, this could not be confirmed. specimen with the cap missing was association. It is, therefore, chiefly found By the time it was realised that this was noticed. As a test of their reaction, the in pine plantations and in association with most probably a case of mushroom intoxi- pups were allowed to roam at will and an exotic trees such as , oaks and cation, the chemical toxicological test on inquisitive individual crawled in under Eucalyptus spp. This introduced mush- the gastric contents of the sick pup had the branches right up to the stem of the room has a cosmopolitan distribution and unfortunately already been completed tree. in South Africa is prevalent in the Eastern and both the specimen and container The owner informed us that, depending and Western Cape Provinces, KwaZulu- discarded. Consequently, no specimen on rain, this particular mushroom had Natal, Gauteng and Mpumalanga26. was available for spore examination. been encountered periodically for years The closely related and morphologically Spores of A. pantherina were not found by on the property but that it had never similar A. muscaria (fly agaric), which flotation in the small amount of faeces of presented any problem. causes the same intoxication, has a bright the 3rd pup. red cap with white warts. It is commonly Description of Amanita pantherina encountered in the Western and Eastern Identification of the probable cause (DC.: Fr.) Gonnerm. & Rabenh., Fig. 1 Cape Provinces, Free State, Gauteng and of intoxication This species (commonly known as the Mpumalanga during the rainy season19,26. The owner was questioned about possi- panther, panther mushroom or warted ble exposure to any known poisonous agaric) has all the characteristics of an substances or medicines but was adamant ordinary mushroom: at the button-stage DISCUSSION that this could not have occurred. She the cap (or pileus) is dome-shaped, then Although the diagnosis could not be was, however, requested to reinvestigate becomes convex and finally flattened confirmed irrefutably in this particular this possibility at home. The day follow- with a slightly upturned, distinctly incident, all indications are that it had ing the intoxication she submitted a striated margin. The colour varies from indeed been a case of A. pantherina intoxi- partially chewed mushroom that had rather pale creamy-brown or grey-brown cation. A chewed mushroom was found been found next to the pups’ run, as well to ochre-brown, sometimes with an olive in the proximity of the puppies’ pen and as whole mushrooms collected from tint. The pileus is covered with persistent, it was evident that the litter had access to under a nearby cedar tree on the property. irregularly dispersed, white volval warts. the mushrooms growing under the

156 0038-2809 Tydskr.S.Afr.vet.Ver. (1997) 68(4): 154–158 A humans3. It is surmised that, in the dog, the equivalent of the extended stage of delirium seen in humans would manifest as a transient disorientation. Fortunately no mortality occurred in this particular case, as opposed to 3 out of 5 pup deaths in the intoxication recorded by Hunt12. The quantity consumed in this instance might have been less. In humans, mortality due to A. panthe- rina is rare18, in spite of the fact that it is the B most common mushroom intoxication encountered in Europe3 and the Pacific North-West23 and that, in all probability, it is the mushroom most commonly used to obtain a psychotropic effect in the United States of America23. In contrast, in con- firmed intoxications in dogs relatively high mortality has been reported12,29. This could perhaps be ascribed to greater Fig. 2: Structural relationship between false (A) from Amanita pantherina sensitivity of young animals (41⁄2 to 51⁄2 and naturally occurring neurotransmitters (B) (adapted from Lampe18). weeks old). and related excitatory amino-acids like ibotenic acid deodar cedar next to their run. It is Renshaw cells, whereas muscimol, like produce convulsions in immature rats in well-known that pups will chew (and GABA, is a powerful inhibitor of firing of which the blood/brain barrier is not sometimes even swallow) peculiar central neurons14. Unlike glutamic acid completely developed (Johnston as cited material, inter alia poisonous metallic and GABA, ibotenic acid and muscimol by Chilton8). However, mature animals substances like lead6 and certain toxic cross the blood/brain barrier, apparently are protected only from the convulsive plants such as Dieffenbachia and even by active transport, and these false neuro- properties of glutamic acid and GABA cycads4. transmitters appear to be the main cause and not from those of muscimol and Failure to find mushroom spores in a of the syndrome (Chilton8 citing Balkar ibotenic acid, which cross the blood/brain small quantity of faeces from the last of and Krogsgaard-Larsen). barrier (Balkar and Johnston and the poisoned pups might be ascribed to The toxin content in this mushroom Krogsgaard-Larsen and Johnston as cited digestion. Examination of gastric contents appears to vary considerably. In a by Chilton8). in this regard would probably have recorded incident of poisoning in humans In the present case, successful general confirmed the intoxication and should be in South Africa, it was estimated that the symptomatic treatment was instituted, as a standard procedure in all cases of adult individuals involved each had only a specific diagnosis had not been made. It suspected mushroom intoxication. In our consumed approximately a tablespoonful consisted of controlling the nervous signs case, however, all the gastric contents of cooked mushroom. This resulted in and stabilising the electrolyte balance. collected from the 1 pup had been used in severe intoxication3. In contrast, in the Where a case of known poisoning by the the test for strychnine and by the time the United States, where this species is widely A. pantherina/A. muscaria-group of mush- diagnosis was made, even the container used for the deliberate induction of a rooms is presented, the serious nervous had been discarded. hallucinogenic state, Ott23 states that ‘half signs should first receive attention, and The hallucinogenic principles in both a cup of sauteed mushrooms is usually then further absorption of toxins A. pantherina and A. muscaria that result in enough’ to produce the desired effect. should be prevented. Great care must be subsequent coma are ibotenic acid and its Apparently the inconsistent transient exercised in the use of sedatives, as the decarboxylation product, muscimol nausea prior to hallucination is no administration of small doses of diaze- (Fig. 2). Both constituents have the same deterrent to the habitual user. However, pam or phenobarbitone in muscimol- pharmacological effects, although musci- in accidental intoxication, this nausea, treated experimental animals induces a mol is 5–10 times more potent than followed by severe, unexpected delirium, flaccid paralysis and an EEG-pattern ibotenic acid29. Contrary to earlier belief, is clearly a most frightening experience. similar to deep anaesthesia28. It is, these mushrooms contain insignificant It is interesting also that the insecticidal therefore, possible that the cardio-respira- amounts of muscarine. They possibly properties of these mushrooms (whence tory arrest in one of the pups in this contain as yet unidentified components the popular names ‘fly agaric’ or ‘Fliegen- incident was induced by the intravenous that may contribute to the intoxication pilze’ for A. muscaria) are also ascribed to administration of diazepam. It is suggested syndrome. However, ibotenic acid and the ibotenic acid and muscimol5. that this could have occurred either as muscimol, together with their metabo- Except for the shorter period of convul- a result of potentiation of the muscimol- lites, appear to be responsible for the signs sions, the signs encountered in the induced GABA effect (i.e. neuro-inhibi- of this poisoning: nausea, hallucinations, current incident were very similar to tion), or due to the inherent hypotensive delirium, muscular and sleep8. those seen in the only other confirmed effect of diazepam2. Further absorption Ibotenic acid is a conformationally field incident of this intoxication in the should be limited by the judicious use of restricted derivative of glutamic acid, as dog12, as well as to those encountered apomorphine (or if this is contra-indi- muscimol is of gamma-aminobutyric acid experimentally with ibotenic acid and cated by the state of consciousness of the (GABA)8. Ibotenic acid, like glutamic acid, muscimol in canines29. The syndrome in patient, gastric lavage), followed by is an excitant of isolated interneurons and dogs also can be equated to that seen in activated charcoal at 2 g/kg.

0038-2809 Jl S.Afr.vet.Ass. (1997) 68(4): 154–158 157 ACKNOWLEDGEMENTS 7. Burton H A 1944 Mushroom poisoning in Journal of Veterinary Diagnostic Investigation cattle. Veterinary Medicine 39: 290 1: 267–269 We gratefully acknowledge Prof. A 8. Chilton W S 1978 Chemistry and mode of 21. Martin J G 1956 Mycetism (mushroom poi- Eicker, Department of Botany, University action of mushroom toxins. In Rumack B H, soning) in a dog: case report. Veterinary of Pretoria, for confirming the identifica- Salzman M D (eds) Mushroom poisoning: Medicine 51: 227–228 tion of the mushrooms, for the faecal diagnosis and treatment. CRC Press, Florida: 22. Mullenax C H, Mullenax P B 1962 Mush- examination, and for constructive criti- 87–124 room poisoning in cats – two possible cases. 9. Cole F M 1993 A puppy death and Amanita Modern Veterinary Practice 43: 61 cism of the manuscript; Prof. R Vleggaar, phalloides. Australian Veterinary Journal 70: 23. Ott J 1978 Recreational use of hallucino- Department of Chemistry, University of 271–272 genic mushrooms in the United States. In Pretoria, for the computerised production 10. Faulstich H, Kommerell B, Wieland T (eds) Rumack B H, Salzman M D (eds) Mushroom of the structural formulae; Mr P P 1980 Amanita toxins and poisoning. Verlag poisoning: diagnosis and treatment. CRC Minnaar, Department of Pharmacology Gerhardt Witzstrock, Baden-Baden Press, Florida: 231–243 11. Galey F D 1990 A case of Scleroderma citrinum 24. Overas J, Ulvund M J, Bakkevig S, Eiken R and Toxicology, for provisional positive poisoning in a miniature Chinese pot-bellied 1979 Poisoning in sheep induced by the identification of the mushroom speci- pig. Veterinary and Human Toxicology 32: mushroom Cortinarius speciosissimus. Acta mens; the Toxicology Section, 392–330 Veterinaria Scandinavica 20: 148–150 Onderstepoort Veterinary Institute, for 12. Hunt R S, Funk A 1977 Mushrooms fatal to 25. 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