Ustilago / Builenbrand

Builenbrand wordt veroorzaakt door de schimmel Ustilago maydis voorkomend op maisplanten. Op de maïs ziet men na infectie met deze schimmel grijsachtige woekeringen, builen, verschijnen. Vooral in de kolf, maar ook bij de aanhechting van blad en stengel kunnen builen voorkomen. Kuilvoer krijgt een grijze kleur, wat het wellicht wat minder aantrekkelijk maakt voor het vee. De sporen van deze brandschimmel zijn bijna altijd in de grond aanwezig en kunnen zich gemakkelijk via water of wind verspreiden. De sporen kunnen wel vier jaar kiemkrachtig blijven.

Alhoewel in de literatuur soms vermeld wordt dat maïsbuilen enigszins giftig zijn, wordt niets gezegd over de mate van giftigheid of over het soort toxine. Giftigheid is vaak een zaak van hoeveelheden. Ook moet onderscheid gemaakt worden tussen de verse plant en het ingekuild product. Mogelijk worden de giftige stoffen onschadelijk gemaakt in het zure kuilmilieu. Volgens Nederlandse deskundigen vormt Ustilago zelf geen toxines. Op de buil kunnen echter wel secundaire schimmels voorkomen zoals Fusarium, Aspergillus en Penicillium, die soms wel gifstoffen produceren.

Onderzoek met melk- en vleesvee aan het ILVO-Dier toonde aan dat het vervoederen van maïskuilvoeder met veel builenbrand geen problemen geeft voor voeropname, melkproductie en -samenstelling, noch voor de diergezondheid of vruchtbaarheid. In enkele gevallen trad enige dagen diarree op bij de overgang naar snijmaïs met builenbrand.

In Mexico worden de aangetaste, onrijpe kolven als een delicatesse gegeten, waar het huitlacoche wordt genoemd. De kolven worden voor dit doel 2 tot 3 weken na infectie geoogst en daarna gekookt. In de aangetaste kolven komen onder andere de smaakstoffen sotolon, vanilline en glucose voor.

Ustilago maydis

Ustilago maydis (previously known as U. zeae) is native to Mexico, but is now distributed almost worldwide wherever the host is cultivated. It was first described in 1815 by de Candolle from France, as Uredo maydis. The economic importance of this species has led to an extensive literature on its biology, taxonomy, and uses. It is an important crop pathogen and a major quarantine pest. Host infection occurs through young tissue above ground, often via wounds, affecting all plant parts and often leading to large, distinctive and conspicuous galls of the host. Control measures mainly involve the use of resistant host varieties and chemical seed treatments. However, the swollen host tissue caused by this smut has long been an important food item, known as huitlacoche in Central America, and is becoming increasingly so in North America. Corn smut is also an important study organism which has been extensively used in genetic research and subjected to detailed study.

Maize smut is the oldest plant disease which is illustrated by drawings, infected maize plants being figured in the Florentine Codex MS prepared soon after the Spanish conquest of Mexico in 1519. The galls were certainly well known to the Aztecs long before the 16th century, and feature in early Mexican mural paintings. The smut was first recorded in Europe in 1768 and then referred to as Lycoperdon zeae, the generic name now applied to puff-balls. In Britain it was first recorded in Dorset in 1850, an observation published by Rev. M.J. Berkeley in the Gardener’s Chronicle.

Used traditionally as human food, especially as soup, maize smut is much prized as a delicacy, and has long been marketed as a food in Mexico. It is of increasing economic importance in North America, and grown more extensively as a cash crop which may be more valuable than the maize itself. The ethnic name for the young galls is huitlacoche. The flesh contains carbohydrates, fats and proteins, and has high levels of essential amino acids, oleic and linoleic acids, and vitamins.

The smut has also had other uses by native Americans, such as inducing labour, due to ustilagine which is similar in its properties to ergotamine obtained from ergots (Claviceps purpurea). It is also valued as a homeopathic remedy, being used, in accordance with the medical descriptions, primarily for diseases of the female reproductive organs.

Valverde, M. E., Paredes-Lopez, O., Pataky, J. K. & Guevara-Lara, F. (1995). Huitlacoche (Ustilago maydis) as a food source ― biology, composition, and production. Critical reviews in food science and nutrition 35: 191 - 229.

The Ustilaginales are specialized to parasitize a number of valuable crop species such as corn, sorghum, wheat and barley. Prominent among this group is Ustilago maydis (sometimes referred to as U. zeae), the etiologic agent of corn smut. U. maydis infection of corn leads to the development of tumor-like growths on the aerial portions of the plant, affecting the growth and viability of the crop [4, 5]. Furthermore, large consumption of contaminated corn has been associated with an alkaloid-like toxidrome in cattle, “the staggers.” Ustilago spp., however, are often used in Latin American cuisine where it is better known as huitlacoche [6]; the fungus is frequently included as an ingredient in tortilla-based dishes.

There is a paucity of literature on the role that Ustilago spp. may play in human disease. A strong association has been described between skin hypersensitivity to spores of smut fungi, including U. maydis, and allergic rhinitis and asthma [4, 7]. Teo reported the case of a 23-year-old Chinese woman with a dermatitis whose skin scraping fungal cultures grew Ustilago spp.; the patient's pet guinea pig was suffering from a scaly rash on its paws which also grew Ustilago spp. [8]. There are very few reports of invasive disease due to Ustilago in humans. One of the earliest cases was reported by Moore et al in 1946 in an adult farmer who died of chronic leptomeningitis; at autopsy fungal elements consistent with Ustilago maydis were found in brain tissue, however no cultures were available [9]. In addition there is a single case report of a central line associated bloodstream infection (CLA-BSI) due to U. maydis [10], and a report of hypersensitivity pneumonitis related to exposure to U. esculenta [11]. CLA-BSI due to Pseudozyma aphidis, a related Ustilagomycete, has been described in a child who consumed large quantities of corn tortilla chips [12]. Furthermore, there are additional reports of invasive disease in immunocompromised hosts due to other edible basidiomycetes, such as the mushroom Volvariella volvacea [13]. There are, however, limited data on invasive infections by organisms of the Ustilago genus in pediatrics. In terms of pathogenesis in the case presented, the most logical explanation seems that the child's peritoneal cavity and catheter became contaminated from insertion of the crayon that may have been colonized with Ustilagomycetes from the environment and the child's oral cavity. While our patient denied consumption of huitlacoche, he did consume other traditional Mexican foods including homemade corn tortillas which would be consistent with this mechanism.

Given the limited data on Ustilago in human disease, formulating specific recommendations for treatment are difficult. Based on the few reports of invasive infection due to Ustilago and related organisms, the minimum inhibitory concentrations tend to be lowest for itraconazole followed by amphotericin and fluconazole [10, 12]. There are no available data on the use of echinocandins in these infections. Itraconazole has been used in the few reports of human infection due to Ustilago spp. and related organisms for which specific antifungal therapy has been prescribed and this influenced our decision to change antifungal agents [8, 12]. It is worth noting that our patient had prompt improvement in symptoms after removal of the peritoneal dialysis catheter, and that device removal may be necessary in the setting of infection with this organism. In addition, the reported case of Ustilago CLA-BSI was treated with catheter removal alone and not systemic antifungals with success [10].

In summary, we report an unusual case of peritonitis in a pediatric patient due to Ustilago spp. While traditionally thought of as only a plant pathogen, there continues to be emerging data that this agent can play a role in human disease. Moreover, this case highlights the importance of considering environmental fungi in clinical practice. Continued research into antifungal options for these organisms is warranted.

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7

8

9

Warady BA, Bashir M, Donaldson LA. Fungal peritonitis in children receiving peritoneal dialysis: a report of the NAPRTCS, Kidney Int , 2000, vol. 58 (pg. 384-389)

Google ScholarCrossRefPubMed

Raaijmakers R, Schroder C, Monnens L, Cornelissen E, Warris A. Fungal peritonitis in children on peritoneal dialysis, Pediatr Nephrol , 2007, vol. 22 (pg. 288-293)

Google ScholarCrossRefPubMed

Bibashi E, Memmos D, Kokolina E, Tsakiris D, Sofianou D, Papadimitriou M. , Clin Infect Dis , 2003, vol. 36 (pg. 927-931)

CrossRefPubMed

Lacazo CdS, Heins-Vaccarri EM, Takahashi de Melood N, Hernandez-ArriagaGL. Basidiomycosis: a review of the literature, Rev Inst Med Trop Sao Paulo , 1996, vol. 38 (pg. 379-390)

Google ScholarCrossRefPubMed

Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, KahmannR. Ustilago maydis as a pathogen, Annu Rev Phytopathol , 2009, vol. 47 (pg. 423-445)

Google ScholarCrossRefPubMed

Valverde ME, Paredes-Lopez O, Pataky JK, Guevara-Lara F. Huitlacoche (Ustilago maydis) as a food source—biology, composition and production, Crit Rev Food Sci Nutr. , 1995, vol. 35 (pg. 191-229)

Google ScholarCrossRefPubMed

Santill 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, vol. 55 (pg. 469-471)

Google ScholarPubMed

Teo LHY, Tay YK. Ustilago species infection in humans, Br J Derm , 2006, vol. 154 (pg. 1096-1097)

Google ScholarCrossRef

Moore M, Russell WO, Sachs E. Chronic leptomeningitis and ependymitis caused by Ustilago, probably U zeae (corn smut), Am J Pathol , 1946, vol. 22 (pg. 761-777)

10

12

13

11

Yoshida K, Suga M, Yamasaki H, Nakamura K, Sato T, Kakishima M, et al. Hypersensitivity pneumonitis due to a smut fungus Ustilago esculenta. Thorax., 1996, vol. 51 (pg. 650-651)

Patel R, Roberts GD, Kelly DG, Walker RC. Central venous catheter infection due to Ustilago species, Clin Infect Dis , 1995, vol. 21 (pg. 1043-1044)

Google ScholarCrossRefPubMed

Lin SS, Pranikoff T, Smith SF, Brandt ME, Gilbert K, Palavecino EL, et al. Central venous catheter infection associated with Pseudozyma aphidis in a child with short gut syndrome, J Med Microbiol , 2008, vol. 57 (pg. 516-518)

Google ScholarCrossRefPubMed

Salit RB, Shea YR, Gea-Banacloche J, Fahle GA, Abu-Asab M, Sugui JA, et al. Death by edible mushroom: first report of Volvariella volvacea as an etiologic agent of invasive disease in a patient following double umbilical cord blood transplantation, J Clin Microbiol. , 2010, vol. 48 (pg. 4329-4332)

Google ScholarCrossRefPubMed