Tilletia tritici/Ustilago

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Code: m201
Latin name: Tilletia tritici / Ustilago nuda/tritici/maydis
Source material: Spores and mycelium
Family: Ustilaginaceae
Common names: Ustilago, Corn smut fungus

Fungi

A fungus, which may result in allergy symptoms in sensitised individuals. It is a major clinical problem to identify the extent to which a mould-sensitive patient´s symptoms may be attributed to IgE-mediated allergy.

Allergen Exposure

Ustilago is a member of the basidomycetes, which number over 20 000 species and are physically the largest and morphologically the most complex fungi. They include mushrooms, puffballs, bracket fungi, rusts, and smuts. Most of this group are microfungi, and many are important allergen sources. Basidiospores occur in the air in high concentrations in many parts of the world, and positive skin tests, RAST, and bronchial reactivity to their extracts have been detected in hypersensitive subjects. (1, 2) 

Ustilago maydis, also known as the corn smut fungus, replaces the normal kernels of the cobs with large distorted tumours. (Although many parts of the plant can be infected, in most instances the kernels are the point of infection. The fungus grows through the kernel and causes hypertrophy and hyperplasia, resulting in the formation of massive smut galls.) The black spores developing in these tumours give the cob a burned, scorched appearance – hence the common name ‘smut’. The mould produces enormous quantities of spores. Other species of Ustilago, of which there are at least 9, are pathogens of oats, wheat, other grasses, and ornamental plants. U. esculenta is a common fungal endophyte of wild rice (Zizania latifolia). (3)

Unlike other basidiomycete fungi, such as mushrooms, this fungus does not have a fruiting body. The large black sac which contains the teliospores drops to the ground, and the spores are spread by the wind. In the spring the spores germinate to form basidia, which produce the basidiospores that are the actual infective agent of the corn. Ustilago maydis is dimorphic, with a unicellular, nonpathogenic form, and a dikaryotic, filamentous, pathogenic form that requires the plant for its growth.

A number of studies have demonstrated that Ustilago is common in the atmosphere.

In a study of 5 different sites in the Delhi metropolis, a total of 98 fungal forms were recorded, of which Cladosporium contributed 25 to 40% of the total airborne fungi, followed by Ustilago (24%), Aspergillus flavus (10-13%), Alternaria (11%) and A. niger (8%). Basidiomycetes contributed 7 to 13% at different sites. (4) Similar findings have been reported in a similar study. (5)

In a study in Spain evaluating the air of an outpatient hospital ward, 22 different types of spores were found, the most numerous being Cladosporium, Ustilago and basidiospores. No significant differences were found between measurements at floor level and at a metre high. (6)

In Portugal, the seasonal distribution of fungal spore concentration in the city of Porto was assessed. The highest airborne spore concentration was found during the summer and the early autumn, while the lowest concentration was registered during the winter. Among the 22 fungal spore types identified, Cladosporium (74.5%), Ganoderma (11.7%), Aspergillaceae (2.9%), Ustilago (2.5%), Coprinus (1.5%), Alternaria (1.3%) and Botrytis (1.3%) were the most frequently found. (7)

In Zagreb, Croatia, Ustilago was found to predominate in aerobiological studies in the month of August. (8)

Ustilago has also been found in Istanbul, in Turkey. (9) In a study in Thessaloniki, Greece, the prevalence of fungal spores recorded in a 15-year period was in the following (descending) order: Cladosporium spp. (72.2%), Alternaria spp. (9.8%), and Ustilago spp. (8.1%). (14) Ustilago has also been shown to be an aeroallergen in Mexico. (10)

In a nationwide aerobiological study now in progress in Saudi Arabia, fungal spores also show distinctive seasonal patterns. In descending order, the most common genera were Cladosporium, Ustilago and Alternaria, with Chaetomium and Ulocladium being consistent but minor components. Basiodiospores and ascospores represented less than 10% of the total spore population, indicative of the dry nature of the climate. (11)

Unripe Corn smut, known as ‘huitlacoche’ in Mexico, is considered a culinary delicacy comparable to mushrooms. Ustilago maydis is also occasionally used in homeopathy as a remedy against a number of ailments.

The spores may accumulate in threshing machines, occasionally creating a potentially explosive smut dust.

The genus Tilletia is a group of smut fungi that infects grasses either systemically or locally. Basic differences exist between the systemically infecting species, such as the common and dwarf bunt fungi, and locally infecting species. Tilletia indica, which causes Karnal bunt on wheat, and Tilletia horrida, which causes rice kernel smut, are two examples of locally infecting species on economically important crops. However, even species on noncultivated hosts can become important when occurring as contaminants in export grain and seed shipments. (12)

Allergen Description

No allergens have been characterised.

Potential Cross-Reactivity

Extensive cross-reactivity between the different individual species of the genus could be expected, (2) but has not been documented to date.

Clinical Experience

IgE-mediated reactions

Ustilago has been reported (uncommonly) to induce symptoms of rhinitis, asthma and endemic regional asthma in sensitised individuals, (13, 14, 15, 16) but its association with human disease is unclear, and very few studies have evaluated its relevance to respiratory allergy. The prevalence of respiratory allergy due to fungi spores is not known precisely, but is estimated at 20 to 30% of atopic patients. (17)

A case of respiratory allergy due to grain smuts was first reported almost 7 decades ago, (18) and a subsequent study reported that approximately 25% of 105 patients tested gave positive reactions to smuts. (19) In a study in Arizona, USA, evaluating sensitisation to 7 airborne fungi in 78 patients with asthma and/or allergic rhinitis through skin-specific IgE tests, 11 patients were shown to be sensitised to Ustilago maydis. (13)

Ustilago may be a more relevant allergen than is indicated by the sparse reports in the medical literature. For example, in a Mexican study of 43 adults (15 to 45 years old, 34 with respiratory allergy) tested for sensitisation to Ustilago maydis, Rhodotorula rubra, Puccinia graminis, Cunhigamella spp. and Zyncephalastrum spp., skin-specific IgE to Ustilago maydis was detected in 26% (and in 12, 12, 9 and 6%, respectively, to the other allergens). The study concluded that these moulds should be tested in allergic patients from farming communities. (7)

In a group in the eastern USA (100 patients with asthma and 100 patients with allergic rhinitis) evaluated for skin-specific IgE to 7 basidiospores (Agaricus campestris, Coprinus micaceus, Fuligo septica, Lycoperdon perlatum, Scleroderma lycoperdoides, Ustilago maydis, and sooty mould) using intradermal tests, 436 immediate reactions were observed in the asthmatic group (4.4 per patient), compared to 129 in the group with rhinitis (1.3 per patient). Late-phase reactions had an opposite profile: the asthmatic group had 66 late-phase reactions or 0.7 per patient, compared to 382 or 3.8 per patient in those with rhinitis. (11)

Contrary to the results of these studies, in a Greek study of 15 airborne fungal spore species, although Ustilago spp. was found in the air and skin-specific IgE to fungal spores was found in 32% of the 1 311 asthmatics tested, skin-specific IgE was detected predominantly for Altemaria species in 177 patients (13.5%), in 98 (7.4%) for Cladosporium, in 65 (5%) for Aspergillus, in 45 (3.4%) for Fusarium, and in 36 (2.7%) for Rhizopus. (14)

In a study in Connecticut, USA, evaluating sensitisation to 30 airborne fungi using skin-specific IgE tests on 100 patients with asthma and/or allergic rhinitis, 50 were shown to be sensitised to Ustilago maydis. (20)

A case of hypersensitivity pneumonitis caused by Ustilago esculenta has been reported. (21) Similarly, a 49-year-old woman was admitted with cough, general fatigue, and dyspnoea on effort. Her hobby was the Japanese traditional handicraft of lacquer-carving, sometimes using smut spores of Ustilago esculenta (identified by the word ‘Makomozumi’ on lacquer ware). A provocation test using Makomozumi was positive. Serum tests demonstrated antibodies to the smut spores. (22)

As Ustilago is predominantly found in crops – in particular, corn – occupational exposure is the main source of exposure and therefore of sensitisation. Occupations involved are farming, animal husbandry, baking, longshoreman’s work, and milling.

Other reactions

Fungal infections by basidiomycetes or agaric fungi are being documented in the medical literature more frequently, especially since the advent of AIDS; but not specifically Ustilago infections. The basidiospores of these fungi are found in the atmosphere and transported by wind, and reach the maxillary sinuses by the nasal route. Many cause signs and symptoms of chronic sinusitis. (23) For example, a central venous catheter infection due to an Ustilago species was reported. (24)

Compiled by Dr Harris Steinman.

References

  1. Vijay HM, Kurup VP. Fungal allergens. In: Lockey RF, Bukantz SC, Bousquet J, eds. Allergens and allergen immunotherapy. 3rd ed. New York: Marcel Dekker, Inc; 2004:223-49.
  2. Horner WE, Helbling A, Salvaggio JE, Lehrer SB. Fungal allergens. Clin Microbiol Rev 1995;8(2):161-79.
  3. You W, Liu Q, Zou K, Yu X, Cui H, Ye Z. Morphological and molecular differences in two strains of Ustilago esculenta. Curr Microbiol 2011;62(1):44-54.
  4. Gupta SK, Pereira BM, Singh AB. Survey of airborne culturable and non-culturable fungi at different sites in Delhi metropolis. Asian Pac J Allergy Immunol 1993;11(1):19-28.
  5. Singh AB, Kumar P. Common environmental allergens causing respiratory allergy in India. Indian J Pediatr 2002;69(3):245-50.
  6. Tormo Molina R, Gonzalo Garijo MA, Munoz Rodriguez AF, Silva Palacios I. Pollen and spores in the air of a hospital out-patient ward. Allergol Immunopathol (Madr) 2002;30(4):232-8.
  7. Oliveira M, Ribeiro H, Abreu I. Annual variation of fungal spores in atmosphere of Porto: 2003. Ann Agric Environ Med 2005;12(2):309-15.
  8. Peternel R, Culig J, Hrga I. Atmospheric concentrations of Cladosporium spp. and Alternaria spp. spores in Zagreb (Croatia) and effects of some meteorological factors. Ann Agric Environ Med 2004;11(2):303-7.
  9. Colakoglu G. Fungal spore concentrations in the atmosphere at the Anatolia quarter of Istanbul, Turkey. J Basic Microbiol 1996;36(3):155-62.
  10. Perez Tovar MP, Castrejon Tovar M, Iza SV, Gonzalez Ibarra M, Miranda Feria AJ. Skin test with aeroallergens untested in Mexico. [Spanish] Rev Alerg Mex 1995;42(5):86-8.
  11. al-Nahdi M, al-Frayh R, Hasnain SM. An aerobiological survey of allergens in al Khobar, Saudi Arabia. Allerg Immunol (Paris) 1989;21(7):278-82.
  12. Carris LM, Castlebury LA, Goates BJ. Nonsystemic bunt fungi--Tilletia indica and T. horrida: a review of history, systematics, and biology. Annu Rev Phytopathol. 2006;44:113-33.
  13. Le Coulant P, Lopes G. Endemic regional asthma caused by sensitization to Ustilago; experimental studies. [French] J Med Bord 1957;134(9):1094-8.
  14. Santilli J, Rockwell WJ, Collins RP. The significance of the spores of the basidiomycetes (mushrooms and their allies) in bronchial asthma and allergic rhinitis. Ann Allergy 1985;55:469-71.
  15. Lima AO. Perennial rhinitis and bronchial asthma caused by sensitization by spores of the Ustilago (pers.) Rost. Hospital (Rio J) 1952;41(5):719-25.
  16. Giannini EH, Northey WT, Leathers CR. The allergenic significance of certain fungi rarely reported as allergens. Ann Allergy 1975;35(6):372-6.
  17. Gioulekas D, Damialis A, Papakosta D, Spieksma F, Giouleka P, Patakas D. Allergenic fungi spore records (15 years) and sensitization in patients with respiratory allergy in Thessaloniki-Greece. J Investig Allergol Clin Immunol 2004;14(3):225-31.
  18. Wittich FW, Stackman FC. A case of respiratory allergy due to inhalation of grain smuts. J Allerg 1937;8:189.
  19. Wittich FW. Further observations on allergy to smuts. J Lancet 1939;59:382-8.
  20. Santilli J, Rockwell WJ, Collins RP. Individual patterns of immediate skin reactivity to mold extracts. Ann Allergy 1990;65:454-8.
  21. Yoshida K, Suga M, Yamasaki H, Nakamura K, Sato T, Kakishima M, Dosman JA, Ando M. Hypersensitivity pneumonitis induced by a smut fungus Ustilago esculenta. Thorax 1996;51(6):650-1.Discussion.656-7.
  22. Fujii Y, Usui Y, Konno K, Atarashi K, Ohtani Y, Inase N, Tanaka T, Yoshizawa Y. A case of hypersensitivity pneumonitis caused by smut spores of Ustilago esculenta. [Japanese] Nihon Kokyuki Gakkai Zasshi 2007;45(4):344-8.
  23. Lacaz Cda S, Heins-Vaccari EM, De Melo NT, Hernandez-Arriagada GL. Basidiomycosis: a review of the literature. Rev Inst Med Trop Sao Paulo 1996;38(5):379-90.
  24. Patel R, Roberts GD, Kelly DG, Walker RC. Central venous catheter infection due to Ustilago species. Clin Infect Dis 1995;21(4):1043-4.

 

As in all diagnostic testing, the diagnosis is made by the physican based on both test results and the patient history.