Toxins of Penicillium Species Used in Cheese Manufacture

Abstract

The known metabolites of strains of Penicillium roqueforti associated with blue-veined cheeses are penicillic acid, roquefortine, isofumigaclavines A and B, PR toxin and related metabolites, mycophenolic acid and siderophores. Of these, penicillic acid and PR toxin, one of the most acutely toxic metabolites of P. roqueforti, are unstable in cheese. Roquefortine, isofumigaclavine A, mycophenolic acid and the siderophore ferrichrome have been detected in blue cheese at low ppm levels. Cyclopiazonic acid is a metabolite of Penicillium caseicolum (P. camembertz), the fungus used in the manufacture of Camembert-type cheeses. Low concentrations of this mycotoxin have been detected in the cheese crusts. Although no acute health hazard can be identified from the presence of these known fungal metabolites in mold-ripened cheeses, there are conflicting reports on the carcinogenicity of P. camemberti cultures and one report on sub-acute toxicity of lipids from an Egyptian blue cheese. There are essentially two species of Penicillium used to manufacture mold-ripened specialty cheeses. Spores of Penicillium roqueforti are inoculated into curd or milk in the production of many varieties of blue cheese, such as Roquefort, Stilton, Danish Blue, Gorgonzola and Gammelost. Penicillium caseicolum, synonymous with Penicillium camemberti and the name used by cheesemakers, Penicillium candidum (51, 76), is employed in the ripening of Brie and Camembert. Less well known are lightly bluish strains of P. camemberti sold in France under the name of Penicillium album for making certain goat cheeses (51). Also, the fungus isolated from an Italian blue-veined cheese, Dolce Verde, was described as being related to Penicillium expansum and not toP. roque forti (1 4). Although there appear to be no reports of toxic effects in humans following consumption of fungally-processed cheese, current scientific interest in mycotoxins has focused increasing attention on the production of toxic metabolites by these Penicillium species. It is of some reassurance to note that neither P. roqueforti nor P. caseicolum form aflatoxins (55,84), nor have aflatoxins B 1 , B 2 , G 1 or G 2 been detected in blue cheese or Camembert-type cheese (13,47,84). Paren-thetically, any cheese may be contaminated with aflatoxin M 1 , originating from metabolism of aflatoxin B 1 present in dairy cattle feed (32,74). Engel and von Milczewski (1 7) extended the screening of fungal cultures to include sterigmatocystin, diacetoxyscirpenol, ochra-toxin A, patulin, penicillic acid, citrinin, and citreo-viridin, in addition to aflatoxins B 1 , B 2 , G 1 , G 2 and M 1 , but none of these mycotoxins were produced by 17 strains of P. roqueforti, 36 of P. caseicolum, and five of P. camemberti. Mintzlaff and Machnik (50) similarly detected no aflatoxins B 1 and G 1 , ochratoxin A, patulin, penicillic acid, citrinin, rubratoxin B, tremortin A or zearalenone in extracts from 16 strains of P. caseicolum and seven strains of P. roqueforti used for cheese manufacture; six of the latter strains were toxigenic to chick embryos. Leistner and Eckardt (43) screened 80 strains of P. roqueforti and 69 strains of P. camemberti isolated from foods and feeds for 20 Penicillium mycotoxins (not including aflatoxins) but only known metabolites of these species (see below) were detected. Many of the strains were cheese starter cultures. METABOLITES AND MYCOTOXINS FROM PENICIL-LIUM ROQUEFORT! Patulin, penicillic acid and citrinin Notwithstanding the negative surveys of Engel and von Milczewski (1 7) and Mintzlaff and Machnik (50) referred to above, patulin and penicillic acid (Fig.