Abstract
Background
Anaphylaxis in response to edible mushrooms is uncommon, and sensitization may be independent of occupational exposure. Globally, Agaricusbisporus is one the most cultivated mushroom species, comprising the button, portobello, and Swiss brown varietals.
Objective
Our aim was to describe a case of anaphylaxis in an older nonatopic patient following ingestion of A bisporus and undertake a review of the literature.
Methods
A 77-year-old female was referred to the allergy clinic with a history of grade 3 hypotensive anaphylaxis following ingestion of a mushroom omelette. Her tryptase level 4 hours following acute symptoms was elevated. She continued to consume all other omelette ingredients with the exception of mushroom. Additional investigations included specific IgE testing as well as comprehensive skin prick testing (SPT) to raw and boiled mushrooms.
Results
One month after her index reaction, the result of SPT to boiled button mushroom was positive. The patient’s baseline tryptase level was normal. The results of further SPT with other commonly available boiled mushrooms (the A bisporus mushrooms portobello and Swiss brown, as well as enoki, oyster, and shiitake mushrooms) were also positive.
A review of the literature revealed 27 other cases, with an average patient age of 28.8 years (range 8-68 years) and no gender predisposition. Cases from Europe (n = 14, 51.8%) and Asia (n = 12, 44.4%) comprised the majority of the reports. A bisporus was reported in more than one-third of the cases (n = 10, 37.1%) from Australia, India, Portugal, Spain, and the United Kingdom. Cross-sensitization among the edible mushroom species was evident for those individuals who were tested, but no clear and consistent pattern was identified. In some cases, further diagnostics identified α-mannosidase, α-trehalose, mannitol, and ribosomal protein as specific mushroom allergens.
Conclusion
Clinicians should be aware of mushroom as a cause for anaphylaxis, especially in nonatopic and de novo presentations.
Key words: Mushroom allergy, Agaricus bisporus, allergen, anaphylaxis
Introduction
Edible mushrooms belong to the fungal kingdom, of which the species Agaricus is the most common. The species Agaricus accounts for up to 38% of global production of mushrooms, which includes members of the species A bisporus (eg, button, portobello and Swiss brown varieties), as well as members of the species Agaricus campestris (eg, field mushroom).1 Other edible mushrooms include enoki (Flammulina filiformis), oyster (Pleurotus ostreatus), porcini (Boletus edulis), matsutake (Tricholoma murrillianum), and shiitake (Lentinus edulis).2
Although exposure to edible mushroom spores (especially in the occupational setting) can lead to sensitization with rhinitis, acute anaphylaxis following mushroom ingestion is uncommon, and with sensitization independent of such exposure.3 Furthermore, other reactions such as oral allergy syndrome or pseudoallergic reactions due to toxin-mediated mechanisms have also been described following mushroom ingestion.4,5
Anaphylaxis in response to edible mushrooms has a reported prevalence of less than 1%, and several factors, such as cultural customs, climate, and geography, are attributed to sensitization.1,2 Here, we report a rare case of anaphylaxis in response to A bisporus in an older nonatopic patient, and we review the literature on anaphylaxis following consumption of edible mushrooms.
Results and discussion
A 77-year-old nonatopic female with a history of anaphylaxis was referred to the allergy clinic. Her medical history included atrial fibrillation, hypertension, and quiescent polymyalgia rheumatica while taking long-term oral prednisolone, 1 mg.
Thirty minutes after consumption of a homemade mushroom omelette (A bisporus, eggs, cow’s milk, and salt), the patient developed rapid-onset dizziness, a sensation of throat tightness, nausea, and generalized urticaria. Her symptoms progressed despite oral antihistamines. No cofactors were identified. She had previously consumed a similar omelette on a regular basis without any incident.
When the ambulance arrived, the patient was agitated, with a Glasgow Coma Scale (GCS) score of 13 (E3V5M5) that rapidly deteriorated to a GCS score of 3 (E1V1M1) with an unrecordable blood pressure and oxygen saturation level. Intramuscular adrenaline in a dose of 500 μg, supplementary oxygen, and fluid bolus were given, eliciting prompt improvement.
In the emergency department, the patient’s GCS score was 15, with erythema of the face and neck documented. She developed urticaria, tongue angioedema, and chest tightness, prompting further intramuscular adrenaline (500 μg), resulting in clinical improvement. An electrocardiogram showed atrial fibrillation without ischaemic changes, and a chest radiograph was normal. The patient’s tryptase level 4 hours following acute symptoms was elevated at 24.8 μg/L (reference range < 11.5 μg/L). She was admitted to the overnight ward; the following day, oxygen was weaned, enabling discharge.
A week later, the patient’s level of mushroom-specific IgE (champignon extract, code F212, ImmunoCAP, Thermofisher, Uppsala, Sweden) was 0.56 kU/L (range 0.1-0.35 kU/L), whereas the results of testing for staple food mix (egg white, milk, fish, wheat, and soybean), nut mix, Alternaria mold, and Cladosporium mold were negative. Her level of total IgE was normal (21 kU/L [reference range < 119 kU/L).
She continued strict mushroom avoidance; egg, cow’s milk, and salt were tolerated. An allergy consultation 1 month after her index reaction revealed a positive result of skin prick testing (SPT) to boiled button mushroom (a 5-mm wheal). A commercial extract for mushroom SPT was not available for testing. The patient’s baseline tryptase level was normal (8.1 μg/L). Further SPT with other commonly available edible mushrooms was arranged several weeks later, with a positive histamine control (a 10 mg/mL). The result of testing for raw oyster mushroom was positive (a 3-mm wheal), whereas the other testing results were negative. All of the boiled mushrooms tested evoked a positive SPT result; the A bisporus mushrooms portobello and Swiss brown elicited a positive reaction (4- and 5-mm wheals, respectively), and testing to enoki, oyster, and shiitake mushrooms resulted in 4-, 5-, and 4-mm wheals, respectively) (Fig 1).
Fig 1.
Results of SPT to raw and cooked mushroom varietals with positive and negative controls.
Herein, we report the first Australian case of hypotensive anaphylaxis in an older adult without occupational exposure in whom sensitization to boiled A bisporus, as well as to other edible mushroom varieties, was confirmed by SPT.
As anaphylaxis in response to edible mushrooms is not common, a review of the literature in the PubMed and Web of Science databases was undertaken. The search terms mushroom + allergy and mushroom + anaphylaxis were used to identify publications up to May 2024. Case reports and case series available as full text were identified; only those with anaphylaxis following consumption of edible mushroom and confirmed sensitization were included. A total of 27 cases were identified; 14 (51.8%) were female and 13 were male. Their average age was 28.8 years (range 8-68 years). Cases from Europe (n = 14, 51.8%) or Asia (n = 12, 44.4%) comprised the majority of the reports. The average Brown grade anaphylaxis score was 2 (range 1-3).6 Three of the case patients had history of reactions to multiple mushroom species (Table I). Overall, A bisporus was reported in more than one-third of the cases (n = 10, 37.0%) from Australia, India, France, Portugal, Spain, and the United Kingdom, followed by Lentinula edodes (n = 5, 18.5%) in the cases from Japan, the United Kingdom, and Spain and Tricholoma matsutake (n = 4, 14.8%) (with all cases of the latter occurring in Japan). The remaining cases involved Boletus badius, Flammulina velutipes, P ostreatus, Auricularia polytrichia, and Hericium erinaceus (Table I).
Table I.
Summary of the reported cases anaphylaxis in response to edible mushrooms
| Case | Country | Age, sex | Mushroom species | Brown grade anaphylaxis | Aeroallergen sensitization | Other food allergy labels | Occupational/ environmental exposure | In vivo testing (SPT) | In vitro testing | Other | Reference∗ |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | Australia | 13 y, M | A bisporus | 2 | Nil | Peanut | Nil | Raw, 6-mm wheal; cooked, 6-mm wheal A campestris: raw, 8-mm wheal; cooked, 6-mm wheal |
Nil | Nil | Ho and Hill, 2006 |
| 2 | Spain | 15 y, F | A bisporus | 2 | Grass pollen, Alternaria, Aspergillus, Cladosporium | Ni | N/A | Raw stem, 11-mm wheal; cap, 7-mm wheal; gill, 6-mm wheal | Total IgE level, 400 kU/L; sIgE level, 0.27kU/L | IgE-reactive protein, 36 kDa – porin Alternaria IgE-reactive protein, also 36 kDa |
Betancor et al, 2020 |
| 3 | Portugal | 17 y, M | A bisporus | Anaphylaxis | Alternaria, Cladosporium | Nil | Nil | Raw, positive reaction | Total IgE level, 264 IU/mL | IgE reactive protein, 30 kDa; FDEIA OCT, negative result | Carrapatoso et al, 2013 |
| 4 | United Kingdom | 20 y, F | A bisporus | 2 | Tree pollens | Nil | N/A | Raw, negative reaction; cooked, 7-mm wheal Ccibarius: raw and cooked, 3-mm wheal Ledodes: raw, 3-mm wheal; cooked, negative reaction Ctubaeformis /Lnuda, P ostreatus: negative reaction (raw and cooked) B edulis: cooked, negative reaction |
Nil | SPT to 10% and 20% mannitol, negative reaction | Kayode et al, 2020 |
| 5 | France | 23 y, M | A bisporus | 1 | Grass and tree pollens, Alternaria, animal dander | Nil | Nil | Cooked, 15-mm wheal | Positive reaction to recombinant testing with aeroallergens | Nil | Herry et al, 2022 |
| 6 | India | 32 y, F | A bisporus | 2 | N/A | Pomegranate | Unknown | Raw, 5-mm wheal; cooked, 3-mm wheal; mannitol, 5-mm wheal | Total IgE level, 200 IU/mL; sIgE testing, negative reaction | Allergen, mannitol | Hedge et al, 2002 |
| 7 | Portugal | 33 y, M | A bisporus | 2 | HDM | Nil | Nil | Extract, 7-mm wheal; White: raw, 9-mm wheal; cooked: 11-mm wheal Brown: raw, 14-mm wheal; cooked, 11-mm wheal |
Total IgE level, 240 kU/L; sIgE level, 0.76 kU/L | IgE-reactive proteins: 10 kDa and 27 kDa | Cunha et al, 2020 |
| 8 | United Kingdom | 36 y, F | A bisporus | 3 | Tree pollens | N/A | N/A | Raw, 5-mm wheal; cooked, 7-mm wheal C cibarius: raw, negative reaction; cooked, 4-mm wheal C tubaeformis, L nuda, L edodes, and P ostreatus: negative reaction (raw and cooked) B edulis: cooked, negative reaction |
Nil | SPT to 10% and 20% mannitol, negative reaction | Kayode et al, 2020 |
| 9 | Spain | 38 y, F | A bisporus | Anaphylaxis |
Alternaria, Aspergillus, Cladosporium, Penicillium |
Rosaceae fruits (OAS) | Nil | Raw, positive reaction; P ostreatus, L edodes, B edulis: raw, positive reaction |
Total IgE level, 271 kU/L; sIgE level, 2.1 kU/L | IgE-reactive proteins, 24 kDa and 27 kDa | Gabriel et al, 2015 |
| 10 | United Kingdom | 68 y, M |
A bisporus, L edodes |
3 |
Alternaria, Aspergillus, Cladosporium, HDM, grass pollens |
N/A | N/A |
A bisporus: raw, 3-mm wheal; cooked, 6-mm wheal L edodes: raw, 4-mm wheal; cooked, 7-mm wheal L nuda: raw, 3-mm wheal; cooked, 8-mm wheal B edulis: cooked, 8-mm wheal C cibarius, C tubaeformis, P ostreatus: negative reaction (raw and cooked) |
Nil | SPT to 10% and 20% mannitol, negative reaction | Kayode et al, 2020 |
| 11 | Japan | 18 y, F |
L edodes Gfrondosa Hmarmoreus |
Anaphylaxis | Nil | Nil | Nil |
L edodes: raw, 4-mm wheal G frondosa: raw, 8-mm wheal H marmoreus: raw, 5-mm wheal |
Nil |
L edodes IgE protein, 15 kDa G frondosa IgE protein, 8 kDa and 9 kDa H marmoreus IgE protein, 10 kDa and 11 kDa |
Ito et al, 2020 |
| 12 | Japan | 21 y, M |
L edodes G frondosa H marmoreus Peryngii |
1 | Grass and tree pollens, HDM, Alternaria, Aspergillus |
L edodes: raw and cooked, 5-mm wheal G frondosa: raw, 12-mm wheal H marmoreus: raw, 9-mm wheal Peryngii: raw, NP F velutipes: raw, 10-mm wheal A auricula: raw, negative reaction |
Total IgE level, 457 IU/mL | L edodes and P eryngii IgE protein, 15 kDa – ribosomal protein S8 and S15a, identified to be cross-reactive with inhibition studies; further testing with G frondosa and H marmoreus not performed | Ogino et al, 2022 | ||
| 13 | United Kingdom | 37 y, M | L edodes | 1 | HDM, silver birch tree pollen | N/A | N/A | Raw, 7-mm wheal; cooked,10-mm wheal P ostreatus: raw, negative reaction; cooked, 4-mm wheal C tubaeformis: raw, 3-mm wheal; cooked, negative reaction A bisporus, C cibarius, L nuda: negative reaction (raw and cooked) |
Nil | SPT to 10% and 20% mannitol: negative reaction | Kayode et al, 2020 |
| 14 | Spain | 36 y, M | L edodes | 1 | Nil | Nil | Nil | Extract, 12-mm wheal; Raw and boiled, 10-mm wheal |
Total IgE level, 17.9 IU/mL | IgE-reactive protein, 19-26.5 kDa Tolerance of other mushrooms: A campestris, C tubaeformis, B edulis |
Romero-Sanchez et al, 2023 |
| 15 | Japan | 8 y, F | T matsutake | 2 | HDM, Japanese cedar pollen | Nil | N/A | Raw: strong positive reaction F velutipes: raw, positive reaction; others (Pnameko, G frondosa, L shimeji, L edodes): negative reaction |
Total IgE level, 504 IU/mL; sIgE level, 2.0FU; tryptase level, 14/5 mg/L | Nil | Ichikawa et al, 2006 |
| 16 | Japan | 27 y, M | T matsutake | 1 | Japanese cedar pollen | Nil | Nil | Extract, positive reaction | Total IgE level, 368 IU/mL; sIgE level, negative reaction | OCT-positive at 100 g): grade 2; tolerance of other mushrooms: F velutipes, L edodes, P ostreatus | Komase et al, 2008 |
| 17 | Japan | 29 y, M | T matsutake | 2 | Nil | Nil | Chef | Raw, 4-mm wheal | Total IgE level, 480 IU/mL | Nil | Amano et al, 2003 |
| 18 | Japan | 38 y, F | T matsutake | 3 | HDM | Nil | N/A | Raw, 5-mm wheal; L edodes: raw, negative reaction | Total IgE level, 178 IU/mL | Histamine release by basophils against extract | Toda et al, 2010 |
| 19 | Germany | 25 y, F | B badius | 2 | Grass pollen, Alternaria, Cladosporium |
Walnut (OAS) | Nil | Raw, 7-mm wheal A bisporus: raw, 4-mm wheal L edodes and P ostreatus: raw, 3-mm wheal B edulis: raw, negative |
Total IgE level, 341 IU/mL | Positive BAT result; B edulis OCT, negative result | Fischer et al, 2017 |
| 20 | Switzerland | 42 y, F | B badius | 3 | Grass pollen | Nil | Nil | Raw and dried, strong positive reaction L edodes, A bisporus, P ostreatus: dried, negative reaction |
RAST result: 0.6 PRU/mL (class 1) | Nil | Torricelli et al, 1997 |
| 21 | Switzerland | 65 y, M | B badius | 3 | Nil | Nil | Nil | Raw and dried, strong positive reaction; A bisporus: dried, positive reaction L edodes and P ostreatus: dried, negative reaction |
Total IgE level, 110kU/L RAST: negative result | Nil | Torricelli et al, 1997 |
| 22 | Japan | 10 y, F | F velutipes | 1 | HDM, dog dander, Candida | Nil | Nil | Raw, 4-mm wheal; cooked, 3-mm wheal L edodes and H marmoreus: raw, 5-mm wheal P eryngii: raw, 5-mm wheal |
Total IgE level, 706 IU/mL | IgE-reactive protein, 75 kDa | Shingaki et al, 2017 |
| 23 | Japan | 17 y, F | F velutipes | 3 | Nil | Nil | Nil | Raw, 5-mm wheal P eryngii: raw, 3-mm wheal L edodes, H marmoreus, P nameko, A bisporus, A auricula: raw, negative reaction |
Total IgE level, normal range | IgE-reactive proteins,18 kDa, 39 kDa, and 50 kDa | Otsuji et al, 2015 |
| 24 | Thailand | 12 y, M | P ostreatus | 2 | HDM | Nil | Nil | Raw, 8.5-mm wheal; cooked, 8.5-mm wheal L edodes: raw, 3-mm wheal; cooked, 3-mm wheal F velutipes: raw, 3-mm wheal; cooked, 4-mm wheal A cornea: raw, negative reaction; cooked, 4-mm wheal P eryngii and V volvacea: negative reaction (raw and cooked) |
Nil | Allergen, trehalose phosporylase (150-250 kDa) P ostreatus OCT, positive result Negative OCT result to P eryngii, L edodes, F velutipes, A cornea, V volvacea |
Rangkakulnuwat et al, 2023 |
| 25 | Korea | 17 y, F | P ostreatus | 2 | HDM, Alternaria | Nil | Nil | Extract: 5.5-mm wheal Extract of others: P eryngii, 7-mm wheal; F filiformis, 3-mm wheal; L edodes, 8.5-mm wheal |
Total IgE level, 205 kU/L | Nil | Seo et al, 2015 |
| 26 | Japan | 37 y, F | A polytricha | 2 | Nil | Cherry, peach (OAS) | Nil | Raw, negative reaction; cooked, 4-mm wheal | Total IgE level, 323 IU/mL | Allergen, α-mannosidase (66 kDa) | Kobayashi et al, 2019 |
| 27 | United States | 43 y, M | H erinaceus | 2 | N/A | N/A | N/A | Extract, negative reaction; raw, 3-mm wheal | Nil | Possible alcohol cofactor | Watson and Kobernick 2022 |
BAT, Basophil activation test; F, female; FDEIA, food-dependent exercise induced anaphylaxis; HDM, house dust mite; M, male; N/A, not available; NP, not performed; OAS, oral allergy syndrome; OCT, oral challenge test; RAST, radioallergosorbent test; sIgE, specific IgE.
For Table I reference list, see the Online Repository (available at www.jaci-global.org).
Of the 27 case patients, 17 had skin testing to other edible mushroom species. Of these case patients, 15 demonstrated sensitization to other mushroom species on SPT; however, no clear and consistent pattern was identified (Table I). For example, in case 19, which involved anaphylaxis in response to B badius with a positive result of SPT to the raw form (a 7-mm wheal), the result of SPT to the other Boletus species (B edulis) was negative, and a subsequent challenge was tolerated despite positive results of SPT to other varieties (L edodes and P ostreatus). In case 8, which involved anaphylaxis in response to A bisporus, the results of SPT to B edulis, P osteratus, and L edodes were also positive; however, B badius was not tested, and no further oral challenge to an alternate edible mushroom variety was undertaken. On the other hand, in case 20, which involved anaphylaxis in response to B badius, the results of SPT to L edodes, A bisporus, and P osteratus were negative, but no challenge was performed.
In our patient, all results of SPT to the 5 boiled mushroom varieties to highlight the presence of heat-resistant proteins were positive. This suggests that unlike many of the proteins such as ovalbumin that are typically denatured by heat, this process may also ensue in emergence of allergenic proteins or neoantigens.7 One example of this process is development of advanced glycation end products described in the Maillard reaction.8,9 These products are resistant to digestion, which may then modify the immune response.7,10 Such a reaction has been described in pecan nut, wheat, and prawn allergy.8,11 In our patient, only 1 variety elicited a positive SPT result when tested in raw form, and while a postulation is that raw prick-to-prick testing was performed to sliced mushroom rather than to a slurry, this has not been confirmed, and in the absence of definitive literature, we cannot conclude this with certainty.
Of the 27 case patients, 13 had further in vitro testing performed; the testing included the basophil activation test and Western blot. Although some potential allergens such α-mannosidase, α-trehalose, mannitol, and ribosomal protein have been postulated, the exact mechanism is not clear given the extensive cross-reactivities and the low number of well-studied cases.12, 13, 14, 15 For example, although in 1 case mannitol was identified as the mushroom allergen following anaphylaxis in response to A bisporus, another case series with 3 patients found the results of SPT to this allergen to be negative.16,17 Of the 27 case patients, 8 had concurrent sensitization to Alternaria and/or Cladosporium molds, which may suggest an attribution to respiratory symptoms and independence of anaphylaxis on ingestion.5 Environmental exposure and respiratory symptoms have been described among the Basidiomycetes, and specific allergens such as Coprinus comatus have been identified in molecular studies, some of which also have cross-reactivity to mushroom spores and common molds.18,19 However, further exploratory studies are required to examine anaphylaxis on consumption, as observed in case 2, in which a patient with a history of anaphylaxis in response to A bisporus and atopy had IgE-reactive protein that was identical to Alternaria at 36 kDA and reported to be a porin.20 In our patient, the results of testing to both molds were negative, with no history of atopy or occupational exposure. Previously, it has been suggested that sensitization may occur during a vulnerable time period, such as during a viral infection or intestinal mucosal inflammation.21
The findings regarding our patient and collective review of cases to date highlight the fact that a large heterogeneity in sensitization patterns is present. In this context, although clear guidelines surrounding cross-sensitization are not possible, our suggestions are to undertake collection of a comprehensive history, including occupational exposure and atopy, followed by skin testing to both raw and cooked forms of mushrooms. It is also recommended that where available, multiple types of edible mushroom species be tested, especially if the patient is showing interest in undergoing challenges for those varietals for which the results of SPT are negative. Testing for specific IgE has limitations in terms of availability, cost, and turnaround times. Additionally, a low level specific IgE did not correlate with clinical severity, as seen in our patient, as well as in patients in several other cases. The role of Western blot and proteomics is largely reserved for the research setting, and no clear unifying IgE-specific protein in the cases has been identified thus far. Finally, consideration also needs to be given to the types of edible mushrooms available in the country, which is of course dependent on geography, climate, and cultural customs.
In summary, anaphylaxis in response to edible mushroom is not common, and clinicians should be aware of it as an allergen. Importantly, patients may have no prior exposure, and as seen in our case, sensitization to edible mushroom can develop de novo, much later in life with severe anaphylaxis. A review of the literature highlights many reports from Japan and European cities, highlighting the fact that local consumption may drive patterns for sensitization. Further molecular diagnostics is required for edible mushroom allergy to clarify a clear allergen.
Key messages.
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•
Anaphylaxis in response to edible mushroom is uncommon and must be considered as a potential cause, particularly in de novo cases.
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•
Cross-sensitization among the mushroom species is not clear; hence, testing should be offered to multiple varietals in both raw and cooked forms.
Disclosure statement
Fundings statement: There was no funding received for this manuscript.
Disclosure of potential conflict of interest: The authors declare that they have no relevant conflicts of interest.
Footnotes
Written consent has been obtained from the patient.
Ethics declaration: This article has been approved by the Central Adelaide Local Health Network Human Research Ethics (reference no. 19284).
Supplementary data
References
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