Effectiveness of environmentally safe food additives and food supplements in an in vitro growth inhibition of significant Fusarium, Aspergillus and Penicillium species

https://doi.org/10.17221/86/2017-PPSCitation:Zabka M., Pavela R. (2018): Effectiveness of environmentally safe food additives and food supplements in an in vitro growth inhibition of significant Fusarium, Aspergillus and Penicillium species. Plant Protect. Sci., 54: 163-173.
download PDF

We tested 38 legislatively recognised substances such as food additives and supplements for antifungal efficacy, with the aim of providing an alternative to synthetic conventional fungicides. These compounds were tested against 9 significant pathogenic fungal species belonging to the significant genera Fusarium, Penicillium, and Aspergillus. Of these compounds, 6 are proposed as potential candidates to provide a complementary alternative to conventional fungicides. Natamycin provided extreme efficacy expressed as MIC50 (5–31 µg/ml), followed by BHA and then BHT, CaNa2EDTA, PABA, and chitosan expressed as MIC50 (0.7–1.9 mg/ml). Safety and antifungal activity were discussed in terms of the mode of action and molecular structure, as well as in terms of potential practical use and legislative requirements for the introduction into practice. We presume that food additives and food supplements are definitely a great source of antifungal compounds. In developed areas of the world (e.g. in the EU), they could represent legislatively recognised compounds, so-called basic substances.

References:
Alakomi H.-L., Paananen A., Suihko M.-L., Helander I. M., Saarela M. (2006): Weakening Effect of Cell Permeabilizers on Gram-Negative Bacteria Causing Biodeterioration. Applied and Environmental Microbiology, 72, 4695-4703  https://doi.org/10.1128/AEM.00142-06
 
Al-Hatmi Abdullah M. S., Meletiadis Joseph, Curfs-Breuker Ilse, Bonifaz Alexandro, Meis Jacques F., De Hoog G. Sybren (2016): In vitro combinations of natamycin with voriconazole, itraconazole and micafungin against clinical Fusarium strains causing keratitis: Table 1.. Journal of Antimicrobial Chemotherapy, 71, 953-955  https://doi.org/10.1093/jac/dkv421
 
Alves N.M., Mano J.F. (2008): Chitosan derivatives obtained by chemical modifications for biomedical and environmental applications. International Journal of Biological Macromolecules, 43, 401-414  https://doi.org/10.1016/j.ijbiomac.2008.09.007
 
Amborabe B.-E., Bonmort J., Fleurat-Lessard P., Roblin G. (2008): Early events induced by chitosan on plant cells. Journal of Experimental Botany, 59, 2317-2324  https://doi.org/10.1093/jxb/ern096
 
Aparicio J.F., Fouces R., Mendes M.V., Olivera N., Martín J.F. (2000): A complex multienzyme system encoded by five polyketide synthase genes is involved in the biosynthesis of the 26-membered polyene macrolide pimaricin in Streptomyces natalensis. Chemistry & Biology, 7: 895–905.
 
Boubakri Hatem, Gargouri Mahmoud, Mliki Ahmed, Brini Faiçal, Chong Julie, Jbara Moez (2016): Vitamins for enhancing plant resistance. Planta, 244, 529-543  https://doi.org/10.1007/s00425-016-2552-0
 
Carvajal Daniel, Alvarez Rafael, Osorio Edison (2016): Chemical variability of essential oils of Protium colombianum from two tropical life zones and their in vitro activity against isolates of Fusarium. Journal of Pest Science, 89, 241-248  https://doi.org/10.1007/s10340-015-0667-x
 
Chang Te-Yang, Hu Miao-Lin (1996): Concentrations and lipid peroxidation in tissues and toxicity of para-aminobenzoic acid fed to rats in drinking water. The Journal of Nutritional Biochemistry, 7, 408-413  https://doi.org/10.1016/S0955-2863(96)00065-4
 
Chowdhary Anuradha, Agarwal Kshitij, Meis Jacques F., Sheppard Donald C (2016): Filamentous Fungi in Respiratory Infections. What Lies Beyond Aspergillosis and Mucormycosis?. PLOS Pathogens, 12, e1005491-  https://doi.org/10.1371/journal.ppat.1005491
 
Correa-Basurto José, Alcántara Iván Vázquez, Espinoza-Fonseca L. Michel, Trujillo-Ferrara José G. (2005): p–Aminobenzoic acid derivatives as acetylcholinesterase inhibitors. European Journal of Medicinal Chemistry, 40, 732-735  https://doi.org/10.1016/j.ejmech.2005.03.011
 
Costa Lucio, G. (2008): Neurotoxicity of pesticides: a brief review. Frontiers in Bioscience, 13, 1240-  https://doi.org/10.2741/2758
 
El Hadrami Abdelbasset, Adam Lorne R., El Hadrami Ismail, Daayf Fouad (2010): Chitosan in Plant Protection. Marine Drugs, 8, 968-987  https://doi.org/10.3390/md8040968
 
Ernst E. (2000): Chelation therapy for coronary heart disease: An overview of all clinical investigations. American Heart Journal, 140, 139-141  https://doi.org/10.1067/mhj.2000.107548
 
Fan L., Eskin M.N.A. (2015): The use of antioxidants in the preservation of edible oils: In Shahidi F. (ed.): Handbook of Antioxidants for Food Preservation. Cambridge, Woodhead Publishing: 373–388.
 
Finney D.J. (1971): Probit Analysis. London, Cambridge University Press.
 
Flora S.J.S., Mittal M., Mehta A. (2008): Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian Journal of Medical Research, 128: 501.
 
Gaby A.R. (2006): Natural remedies for scleroderma. Alternative Medicine Review, 11: 188.
 
GOODMAN D, MCDONNEL J, NELSON H, VAUGHAN T, WEBER R (1990): Chronic urticaria exacerbated by the antioxidant food preservatives, butylated hydroxyanisole (BHA) and butylated hydroxytoluene (BHT). Journal of Allergy and Clinical Immunology, 86, 570-575  https://doi.org/10.1016/S0091-6749(05)80214-3
 
Goy Rejane C., Britto Douglas de, Assis Odilio B. G. (2009): A review of the antimicrobial activity of chitosan. Polímeros, 19, 241-247  https://doi.org/10.1590/S0104-14282009000300013
 
Gubbins Paul O., Heldenbrand Seth (2010): Clinically relevant drug interactions of current antifungal agents. Mycoses, 53, 95-113  https://doi.org/10.1111/j.1439-0507.2009.01820.x
 
Hachem R., Bahna P., Hanna H., Stephens L. C., Raad I. (2006): EDTA as an Adjunct Antifungal Agent for Invasive Pulmonary Aspergillosis in a Rodent Model. Antimicrobial Agents and Chemotherapy, 50, 1823-1827  https://doi.org/10.1128/AAC.50.5.1823-1827.2006
 
Hancock R E, Wong P G (1984): Compounds which increase the permeability of the Pseudomonas aeruginosa outer membrane.. Antimicrobial Agents and Chemotherapy, 26, 48-52  https://doi.org/10.1128/AAC.26.1.48
 
Juneja Vijay K., Dwivedi Hari P., Yan Xianghe (2012): Novel Natural Food Antimicrobials. Annual Review of Food Science and Technology, 3, 381-403  https://doi.org/10.1146/annurev-food-022811-101241
 
Kahl Regine, Kappus Hermann (1993): Toxikologie der synthetischen Antioxidantien BHA und BHT im Vergleich mit dem nat�rlichen Antioxidans Vitamin E. Zeitschrift f�r Lebensmittel-Untersuchung und -Forschung, 196, 329-338  https://doi.org/10.1007/BF01197931
 
Kean T., Thanou M. (2010): Biodegradation, biodistribution and toxicity of chitosan. Advanced Drug Delivery Reviews, 62, 3-11  https://doi.org/10.1016/j.addr.2009.09.004
 
Kim J.H., Campbell B.C., Mahoney N., Chan K.L., Molyneux R.J., Xiao C.L. (2010): Use of chemosensitization to overcome fludioxonil resistance in Penicillium expansum. Letters in Applied Microbiology, , no-no  https://doi.org/10.1111/j.1472-765X.2010.02875.x
 
Lee Choon Geun, Koo Ja Choon, Park Jae Kweon (2016): Antifungal Effect of Chitosan as Ca 2+ Channel Blocker. The Plant Pathology Journal, 32, 242-250  https://doi.org/10.5423/PPJ.OA.08.2015.0162
 
Muraosa Yasunori, Oguchi Misato, Yahiro Maki, Watanabe Akira, Yaguchi Takashi, Kamei Katsuhiko (2017): Epidemiological Study of <I>Fusarium</I> Species Causing Invasive and Superficial Fusariosis in Japan. Medical Mycology Journal, 58, E5-E13  https://doi.org/10.3314/mmj.16-00024
 
Nakanishi Tsuyoshi (2007): Potential Toxicity of Organotin Compounds via Nuclear Receptor Signaling in Mammals. JOURNAL OF HEALTH SCIENCE, 53, 1-9  https://doi.org/10.1248/jhs.53.1
 
Niessen Ludwig (2007): PCR-based diagnosis and quantification of mycotoxin producing fungi. International Journal of Food Microbiology, 119, 38-46  https://doi.org/10.1016/j.ijfoodmicro.2007.07.023
 
Palumbo Jeffrey D., O'Keeffe Teresa L., Abbas Hamed K. (2008): MICROBIAL INTERACTIONS WITH MYCOTOXIGENIC FUNGI AND MYCOTOXINS. Toxin Reviews, 27, 261-285  https://doi.org/10.1080/15569540802416301
 
Roman Pavela (2016): History, presence and perspective of using plant extracts as commercial botanical insecticides and farm products for protection against insects – a review. Plant Protection Science, 52, 229-241  https://doi.org/10.17221/31/2016-PPS
 
Potshangbam Momota, Devi S. Indira, Sahoo Dinabandhu, Strobel Gary A. (2017): Functional Characterization of Endophytic Fungal Community Associated with Oryza sativa L. and Zea mays L.. Frontiers in Microbiology, 8, -  https://doi.org/10.3389/fmicb.2017.00325
 
Prajna Namperumalsamy V. (2010): Comparison of Natamycin and Voriconazole for the Treatment of Fungal Keratitis. Archives of Ophthalmology, 128, 672-  https://doi.org/10.1001/archophthalmol.2010.102
 
Race S. (2009): Antioxidants: the Truth about BHA, BHT, TBHQ and other Antioxidants Used as Food Additives. Rievaulx, Tigmor Books: 6–11.
 
Ollé Resa Carolina P., Jagus Rosa J., Gerschenson Lía N. (2014): Natamycin efficiency for controlling yeast growth in models systems and on cheese surfaces. Food Control, 35, 101-108  https://doi.org/10.1016/j.foodcont.2013.06.049
 
Sardesai V. (2011): Introduction to Clinical Nutrition. Boca Raton, CRC Press.
 
Scordino Monica, Sabatino Leonardo, Traulo Pasqualino, Gagliano Giacomo, Gargano Maria, Pantò Valentina, Gambino Grazia Laura (2008): LC/MS/MS detection of fungicide guazatine residues for quality assessment of commercial citrus fruit. European Food Research and Technology, 227, 1339-1347  https://doi.org/10.1007/s00217-008-0849-3
 
Simonetti G. (): Enhanced contact activity of fluconazole in association with antioxidants against fluconazole-resistant organisms. Journal of Antimicrobial Chemotherapy, 50, 257-259  https://doi.org/10.1093/jac/dkf102
 
Simonetti Giovanna, Simonetti Nicola, Villa Adelaide (2003): Increase of activity of tioconazole against resistant microorganisms by the addition of butylated hydroxyanisole. International Journal of Antimicrobial Agents, 22, 439-443  https://doi.org/10.1016/S0924-8579(03)00120-1
 
Singh V., Kaushik N.K., Singh R. (2011): Metallosulpha drugs: synthesis and bioactivity. Asian Journal of Research in Chemistry, 4: 339–347.
 
Song Geun Cheol, Choi Hye Kyung, Ryu Choong-Min (2013): The folate precursor para-aminobenzoic acid elicits induced resistance against Cucumber mosaic virus and Xanthomonas axonopodis. Annals of Botany, 111, 925-934  https://doi.org/10.1093/aob/mct049
 
Sonwalkar S.A., Holbrook I.B., Phillips I., Kelly S.M. (2003): A prospective, comparative study of the para-aminobenzoic acid test and faecal elastase 1 in the assessment of exocrine pancreatic function. Alimentary Pharmacology & Therapeutics, 17: 467–471.
 
Welscher Yvonne M. te, Napel Hendrik H. ten, Balagué Miriam Masià, Souza Cleiton M., Riezman Howard, de Kruijff Ben, Breukink Eefjan (2008): Natamycin Blocks Fungal Growth by Binding Specifically to Ergosterol without Permeabilizing the Membrane. Journal of Biological Chemistry, 283, 6393-6401  https://doi.org/10.1074/jbc.M707821200
 
te Welscher Y. M., Jones L., van Leeuwen M. R., Dijksterhuis J., de Kruijff B., Eitzen G., Breukink E. (2010): Natamycin Inhibits Vacuole Fusion at the Priming Phase via a Specific Interaction with Ergosterol. Antimicrobial Agents and Chemotherapy, 54, 2618-2625  https://doi.org/10.1128/AAC.01794-09
 
Thanou M, Verhoef J.C, Junginger H.E (2001): Oral drug absorption enhancement by chitosan and its derivatives. Advanced Drug Delivery Reviews, 52, 117-126  https://doi.org/10.1016/S0169-409X(01)00231-9
 
Van de Sande M.M., Wirtz S., Vos E., Verhagen H. (2014): Short review of calcium disodium ethylene diamine tetra acetic acid as a food additive. European Journal of Food Research & Review, 4: 408.
 
Wang Quansheng, Wei Peng, Cao Mengchao, Liu Yanan, Wang Mengcen, Guo Yirong, Zhu Guonian (2016): Residual behavior and risk assessment of the mixed formulation of benzene kresoxim-methyl and fluazinam in cucumber field application. Environmental Monitoring and Assessment, 188, -  https://doi.org/10.1007/s10661-016-5345-9
 
Wong Tracy, Orton David (2011): Sunscreen allergy and its investigation. Clinics in Dermatology, 29, 306-310  https://doi.org/10.1016/j.clindermatol.2010.11.002
 
Woodward K.N. (2012): Antifungal Drugs: In Toxicological Effects of Veterinary Medicinal Products in Humans. Royal Society of Chemistry: 71–94.
 
Younes Islem, Rinaudo Marguerite (2015): Chitin and Chitosan Preparation from Marine Sources. Structure, Properties and Applications. Marine Drugs, 13, 1133-1174  https://doi.org/10.3390/md13031133
 
Zabka Martin, Pavela Roman (2013): Antifungal efficacy of some natural phenolic compounds against significant pathogenic and toxinogenic filamentous fungi. Chemosphere, 93, 1051-1056  https://doi.org/10.1016/j.chemosphere.2013.05.076
 
Zabka Martin, Pavela Roman, Slezakova Ludmila (2009): Antifungal effect of Pimenta dioica essential oil against dangerous pathogenic and toxinogenic fungi. Industrial Crops and Products, 30, 250-253  https://doi.org/10.1016/j.indcrop.2009.04.002
 
Zabka Martin, Pavela Roman, Gabrielova-Slezakova Ludmila (2011): Promising antifungal effect of some Euro-Asiatic plants against dangerous pathogenic and toxinogenic fungi. Journal of the Science of Food and Agriculture, 91, 492-497  https://doi.org/10.1002/jsfa.4211
 
Zabka Martin, Pavela Roman, Prokinova Evzenie (2014): Antifungal activity and chemical composition of twenty essential oils against significant indoor and outdoor toxigenic and aeroallergenic fungi. Chemosphere, 112, 443-448  https://doi.org/10.1016/j.chemosphere.2014.05.014
 
Zarn Jürg A., Brüschweiler Beat J., Schlatter Josef R. (2002): Azole Fungicides Affect Mammalian Steroidogenesis by Inhibiting Sterol 14α-Demethylase and Aromatase. Environmental Health Perspectives, 111, 255-261  https://doi.org/10.1289/ehp.5785
 
download PDF

© 2020 Czech Academy of Agricultural Sciences