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Public Health Significance of Molds and Mycotoxins in Fermented Dairy Products

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      Abstract

      Mold growth on cheese and other fermented dairy products is a common and recurring problem. Potential mycotoxin contamination is serious since some molds can grow and produce mycotoxins at temperatures as low as −2 to 10°C. Work can be divided into: 1) incidence, types, and mycotoxin-producing potential of molds in fermented dairy products, 2) experimental mycotoxin production on cheese under conditions of storage and aging of cheese, 3) natural occurrence of mycotoxins in commercial samples of cheese, and 4) potential toxicity of Penicillium roqueforti and its significance in blue veined cheeses.
      Molds most common on cheese and fermented dairy products are Penicillium species. Mycotoxins produced by these organisms are penicillic acid, patulin, ochratoxin A, and citrinin. Percentages of molds in cheese capable of producing some commonly studied mycotoxins ranged from 1.8% to 12.4%. Cheese is an excellent substrate for mold growth but a poor substrate for mycotoxin production. Several natural occurrences of mycotoxins in cheese include small and variable amounts of patulin, penicillic acid, sterigmatocystin (600 µg/kg), penitrem A, and mycophenolic acid. Penicillium roqueforti is capable of producing toxic alkaloids and other compounds. The significance of these substances for human health is unclear.
      The decision to trim or to discard moldy cheese can be aided by considering the risk versus benefit based on storage history (temperature), extent of mold growth, appearance of mold (color), and size of cheese.

      References

        • Abdel Kader M.M.
        • Zaki A.H.
        • El-Kirdassy Z.H.M.
        • El-Kammah B.
        • Bosseila A.A.
        An aspect on the nutritive value of Roquefort cheese.
        J. Egypt Med. Assoc. 1969; 52: 764
        • Abdel Kader M.M.
        • Zaki A.H.
        • El-Kirdassy Z.H.M.
        • Shoeb Z.E.
        • Eissa M.H.
        Studies on the toxicity of Roquefort cheese lipids.
        Grasas Aceites. 1970; 21: 197
        • Arp L.H.
        • Richard J.L.
        Intoxication of dogs with the mycotoxin penitrem A.
        J. Am. Vet. Med. Assoc. 1979; 175: 565
        • Bullerman L.B.
        Examination of Swiss cheese for incidence of mycotoxin producing molds.
        J. Food Sci. 1976; 41: 26
        • Bullerman L.B.
        Toxigenic potential of molds isolated from moldy cheese trimmings.
        in: Abstr. 63rd Annu. Mtg., Int. Assoc. Milk, Food, Environ. Sanit. Inc., Arlington Heights, IL1976: 10
        • Bullerman L.B.
        Significance of mycotoxins to food safety and human health.
        J. Food Prot. 1980; 42: 65
        • Bullerman L.B.
        Incidence of mycotoxic molds in domestic and imported cheeses.
        J. Food Safety. 1980; 2: 47
        • Bullerman L.B.
        • Olivigni F.J.
        Mycotoxin-producing potential of molds isolated from Cheddar cheese.
        J. Food Sci. 1974; 39: 174
        • Ciegler A.
        • Kurtzman C.P.
        Penicillic acid production by blue-eye fungi on various agricultural commodities.
        Appl. Microbiol. 1970; 20: 761
        • Ciegler A.
        • Beckwith A.C.
        • Jackson L.K.
        Teratogenicity of patulin and patulin adducts formed with cysteine.
        Appl. Environ. Microbiol. 1976; 31: 664
        • Ciegler A.
        • Mintzlaff H.J.
        • Weisleder D.
        • Leistner L.
        Potential production and detoxification of penicillic acid in mold fermented sausage (salami).
        Appl. Microbiol. 1972; 24: 114
        • Ciegler A.
        • Pitt J.I.
        Survey of the genus Penicillium for tremorgenic toxin production.
        Mycopathologia. 1970; 42: 119
        • Corbion B.
        • Fremy J.M.
        Recherche des aflatoxines B1 et M1 dans les fromages de type Camembert.
        Le Lait. 1978; 58: 133
        • Diener U.L.
        • Davis N.D.
        Limiting temperature and relative humidity for growth and production of aflatoxin and free fatty acids by Aspergillus flavus in sterile peanuts.
        J. Am. Oil Chem. Soc. 1967; 44: 259
        • Diener U.L.
        • Davis N.D.
        Aflatoxin formation by Aspergillus flavus.
        in: Goldblatt L.A. Aflatoxin. Academic Press, New York, NY1969
        • Engel G.
        Studies on the production of mycotoxins and their quantitative determination. 7. Synthesis of aflatoxins by Aspergillus flavus and Aspergillus parasiticus in the presence of sucrose or lactate as C-sources.
        Kiel. Milchwirtsch. Forschungsber. 1976; 28: 385
        • Expert Panel on Food Safety, Nutrition
        The risk/benefit concept as applied to food.
        Inst. Food Technol., Chicago, IL1978
        • Frank H.K.
        Diffusion of aflatoxins in foodstuffs.
        J. Food Sci. 1968; 33: 98
        • Frazier W.C.
        • Westhoff D.C.
        Food microbiology.
        3rd ed. McGraw-Hill Book Co., Inc., New York, NY1978
        • Harwig J.
        • Chen Y.K.
        • Collins-Thompson D.L.
        Stability of ochratoxin A in beans during canning.
        Can. Inst. Food Sci. Technol. J. 1974; 7: 288
        • Hofmann K.
        • Mintzlaff H.J.
        • Alperden I.
        • Leistner L.
        Untersuchung uber die Inaktivierung des Mycotoxins Patulin durch Sulfhydrylgruppen.
        Die Fleischwirtschaft. 1971; 51: 1534
        • Jarvis B.
        Factors affecting the production of mycotoxins.
        J. Appl. Bacteriol. 1971; 34: 199
        • Kanota K.
        Studies on toxic metabolites of Penicillium roqueforti.
        in: Proc. of the First US Japan Conference on Toxic Microorganisms, US Dept. Interior, Washington, DC1970: 129
        • Kiermeier F.
        • Behringer G.
        Influence of cool temperatures on aflatoxin formation in milk products.
        Z. Lebensm. Unters. Forsch. 1977; 164: 283
        • Kiermeier F.
        • Groll D.
        Zur Aflatoxin B1 bilding in Kasen.
        Z. Lebensm. Unters. Forsch. 1970; 143: 81
        • Kiermeier F.
        • Weiss G.
        • Behringer G.
        • Miller M.
        • Ranfft K.
        Vorkommen und Gehalt an Aflatoxin M1 in Molkerei-Anlieferungsmilch.
        Z. Lebensm. Unters. Forsch. 1977; 163: 171
      1. Lafont, P., M. G. Siriwardana, and J. Lafont. 1980. Contamination de fromages par des metabolites fongiques. Ann. Nutr. Alim. (In press).

        • Lafont P.
        • Debeaupuis J.P.
        • Gaillardin M.
        • Payen J.
        Production of mycophenolic acid by Penicillium roqueforti strains.
        Appl. Environ. Microbiol. 1979; 37: 365
        • Lafont P.
        • Lafont J.
        • Payen J.
        • Chany E.
        • Bertin G.
        • Frayssinet C.
        Toxin production by 50 strains of Penicillium used in the cheese industry.
        Food Cosmet. Toxicol. 1976; 14: 137
      2. LaGrange, W. 1979. Moldy cheese – throw or keep? Dairy Ind. Rep. Food Technol., Coop. Ext. Serv. FT–103. Iowa State University, Ames.

        • Leistner L.
        • Pitt J.I.
        Miscellaneous Penicillium toxins.
        in: Rodricks J.V. Hesseltine C.W. Mehlman M.A. Mycotoxins in human and animal health. Pathotox Publ., Inc., Park Forest South, IL1977
        • Levi C.P.
        • Trenk H.L.
        • Mohr H.K.
        Study of the occurrence of ochratoxin A in green coffee beans.
        J. Assoc. Offic. Anal. Chem. 1974; 57: 866
        • Lie J.L.
        • Marth E.H.
        Formation of aflatoxin in Cheddar cheese by Aspergillus flavus and Aspergillus parasiticus.
        J. Dairy Sci. 1967; 50: 1708
        • Lieu F.Y.
        • Bullerman L.B.
        Production and stability of aflatoxins, penicillic acid, and patulin in several substrates.
        J. Food Sci. 1977; 42: 1222
        • Lieu F.Y.
        • Bullerman L.B.
        Binding of patulin and penicillic acid to glutathione and cysteine and toxicity of the resulting adducts.
        Milchwissenschaft. 1978; 33: 16
        • Marth E.H.
        Dairy products.
        in: Beuchat L.R. Food and beverage mycology. AVI Publishing Co., Inc., Westport, CT1978
        • Maxcy R.B.
        Temperatures of water in household refrigerators.
        J. Food Prot. 1979; 42: 124
        • Nickerson J.T.
        • Sinskey A.J.
        Microbiology of foods and food processing.
        Am. Elsevier Publ. Co., New York, NY1972
        • Northolt M.D.
        • VanEgmond H.P.
        • Paulsch W.E.
        Patulin production by some fungal species in relation to water activity and temperature.
        J. Food Prot. 1978; 41: 885
        • Northolt M.D.
        • VanEgmond H.P.
        • Paulsch W.E.
        Penicillic acid production by some fungal species in relation to water activity and temperature.
        J. Food Prot. 1979; 42: 476
        • Northolt M.D.
        • VanEgmond H.P.
        • Paulsch W.E.
        Ochratoxin A production by some fungal species in relation to water activity and temperature.
        J. Food Prot. 1979; 42: 485
        • Northolt M.D.
        • vanEgmond H.P.
        • Soentoro P.
        • Deijll E.
        Fungal growth and the presence of sterigmatocystin in hard cheese.
        J. Assoc. Offic. Anal. Chem. 1980; 63: 115
        • Oldham L.S.
        • Oehme F.W.
        • Kelly D.C.
        Production of aflatoxin in prepackaged luncheon meat and cheese at refrigerator temperatures.
        J. Milk Food Technol. 1971; 34: 349
        • Olson N.F.
        Moldy cheese – what should consumers do with it?.
        Dairy Ice Cream Field. 1979; 162: 82C
        • Olivigni F.J.
        • Bullerman L.B.
        Simultaneous production of penicillic acid and patulin by a Penicillium species isolated from Cheddar cheese.
        J. Food Sci. 1977; 42: 1654
        • Olivigni F.J.
        • Bullerman L.B.
        Production of penicillic acid and patulin by an atypical Penicillium roqueforti.
        Appl. Environ. Microbiol. 1978; 35: 435
        • Park K.Y.
        • Bullerman L.B.
        Increased aflatoxin production by Aspergillus parasiticus under conditions of cycling temperatures.
        in: Abst. 40th Annu. Mtg., Inst. Food Technol., New Orleans, LA1980
        • Pohland A.E.
        • Allen R.
        Stability studies with patulin.
        J. Assoc. Offic. Anal. Chem. 1970; 53: 688
        • Pohlmeier M.M.
        • Bullerman L.B.
        Ochratoxin production by a Penicillium species isolated from cheese.
        in: Abst. 65th Annu. Mtg., Int. Assoc. Milk, Food, and Environ. Sanit. Inc., Kansas City, MO1978
        • Polzhofer K.
        Aflatoxinbestimmung in Milch und Milchprodukten.
        Z. Lebensm. Unters. Forsch. 1977; 163: 175
        • Polzhofer K.
        Modellversuche zur Aflatoxinbildung in Schimelzkase.
        Z. Lebensm. Unters. Forsch. 1977; 164: 94
        • Price R.
        The Arizona scare.
        in: 74th Annu. Mtg, Am. Dairy Sci. Assoc, Logan, UT, June 24–271979
        • Raper K.B.
        • Thom C.
        A manual of the penicillia.
        Hafner Publ. Co., New York, NY1968
        • Richard J.L.
        • Arp L.H.
        Natural occurrence of the mycotoxin penitrem A in moldy cream cheese.
        Mycopathologia. 1979; 67: 107
      3. Rothenbuhler, E., and M. Bachman. 1970. Untersuchungen zum Problem der Aflatoxinbilding in Kase. Schweiz. Milchztg. 96 (74) Wissenschaftliche Beilage 123:1053.

        • Schindler A.F.
        Temperature limits for production of aflatoxin by twenty-five isolates of Aspergillus flavus and Aspergillus parasiticus.
        J. Food Prot. 1977; 40: 39
        • Schindler A.F.
        • Palmer J.G.
        • Eisenberg W.V.
        Aflatoxin production by Aspergillus flavus as related to various temperature.
        Appl. Microbiol. 1967; 15: 1006
        • Scott P.M.
        Penicillium mycotoxins.
        Mycotoxic fungi, mycotoxins, mycotoxicoses. An encyclopedia handbook. Vol. I. Mycotoxic fungi and chemistry of mycotoxins. Marcel Dekker, New York, NY1977
        • Scott P.M.
        • Sommers E.
        Stability of patulin and penicillic acid in fruit juice and flour.
        J. Agr. Food Chem. 1968; 16: 483
        • Scott P.M.
        • Kennedy B.P.C.
        Analysis of blue cheese for roquefortine and other alkaloids from Penicillium roqueforti.
        J. Agric. Food Chem. 1976; 24: 865
        • Scott P.M.
        • Kennedy B.P.C.
        • Harwig J.
        • Blanchfield B.J.
        Study of conditions for production of roquefortine and other metabolites of Penicillium roqueforti.
        Appl. Environ. Microbiol. 1977; 33: 249
        • Shih C.N.
        • Marth E.H.
        Experimental production of aflatoxin on brick cheese.
        J. Milk Food Technol. 1972; 35: 585
      4. Smink, R. 1979. Personal communication.

        • Sorenson W.G.
        • Hesseltine C.W.
        • Shotwell O.L.
        Effect of temperature on production of aflatoxin on rice by Aspergillus flavus.
        Mycopathol. Mycol. Appl. 1967; 33: 49
        • Still P.E.
        • Wei R.D.
        • Smalley E.B.
        • Strong F.M.
        A mycotoxin from Penicillium roqueforti isolated from toxic cattle feed.
        Fed. Proc. 1972; 31: 733
        • Stott W.T.
        • Bullerman L.B.
        Influence of carbohydrate and nitrogen source on patulin production by Penicillium patulum.
        Appl. Microbiol. 1975; 30: 85
        • Stott W.T.
        • Bullerman L.B.
        Instability of patulin in Cheddar cheese.
        J. Food Sci. 1976; 41: 201
        • Torrey G.S.
        • Marth E.H.
        Isolation and toxicity of molds from foods stored in homes.
        J. Food Prot. 1977; 40: 187
        • Torrey G.S.
        • Marth E.H.
        Temperatures in home refrigerators and mold growth at refrigeration temperatures.
        J. Food Prot. 1977; 40: 393
        • Trenk H.L.
        • Butz M.E.
        • Chu F.S.
        Production of ochratoxins in different cereal products by Aspergillus ochraceus.
        Appl. Microbiol. 1971; 21: 1032
        • Tsubaki K.
        Penicillium isolated from toxic ensilage.
        Trans. Mycol. Soc. 1956; (Japan 1): 6
        • van Walbeek W.
        • Clademenos T.
        • Thatcher F.S.
        Influence of refrigeration on aflatoxin production by strains of Aspergillus flavus.
        Can. J. Microbiol. 1969; 15: 629
      5. Wallen, S. E., and L. B. Bullerman. 1978. Safe handling and storage of natural cheeses. NebGuide G 78–403 Coop. Ext. Serv., Inst. Agric. Nat. Res., Univ. Nebraska, Lincoln.

        • Wei R.D.
        • Liu G.X.
        PR toxin production in different Penicillium roqueforti strains.
        Appl. Environ. Microbiol. 1978; 35: 787
        • Wei R.D.
        • Still P.E.
        • Smalley E.B.
        • Schnoes H.K.
        • Strong F.M.
        Isolation and partial characterization of a mycotoxin from Penicillium roqueforti.
        Appl. Microbiol. 1973; 25: 111
        • Wilson B.J.
        Miscellaneous Penicillium toxins.
        in: Microbial toxins. Vol. VI. Academic Press Inc., New York, NY1971