Potential of lactic acid bacteria in aflatoxin risk mitigation

International Journal of Food Microbiology

Volumn 207, Issue , 2015, Pages 87-102

  Ahlberg, Sara H ^a,b   Joutsjoki, Vesa ^a   Korhonen, Hannu J ^a  

^a FINNISH FOREST RESEARCH INSTITUTE   (Finland)

^b INTERNATIONAL LIVESTOCK RESEARCH INSTITUTE   (Kenya)

Author keywords

Aflatoxins; Binding; Fungal growth; Lactic acid bacteria

Indexed keywords

AFLATOXIN; AFLATOXIN B1; AFLATOXIN M1;

ASPERGILLUS FUMIGATUS; ASPERGILLUS OCHRACEUS; BACTERIAL METABOLISM; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM LONGUM; CACO 2 CELL LINE; CULTURE MEDIUM; FOOD CHAIN; FOOD CONTAMINATION; FUNGAL CONTAMINATION; FUNGUS GROWTH; GROWTH INHIBITION; LACTIC ACID BACTERIUM; LACTOBACILLUS; LACTOBACILLUS AMYLOVORUS; LACTOBACILLUS FERMENTUM; LACTOBACILLUS JOHNSONII; LACTOBACILLUS PARACASEI; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; LACTOCOCCUS; LACTOCOCCUS LACTIS; LACTOCOCCUS LACTIS SUBSP. DIACETYLACTIS; LEUCONOSTOC; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PEDIOCOCCUS; PEDIOCOCCUS ACIDILACTICI; PENICILLIUM VERRUCOSUM; PROPIONIBACTERIUM FREUDENREICHII; PROPIONIBACTERIUM FREUDENREICHII SHERMANII; REVIEW; STREPTOCOCCUS THERMOPHILUS; TOXIN SYNTHESIS; ANIMAL; FOOD CONTROL; FUNGUS; METABOLISM; PHYSIOLOGY; PREVENTION AND CONTROL; PROCEDURES; RISK; SPECIES DIFFERENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); FUNGI;

AFLATOXIN B1; AFLATOXINS; ANIMALS; FOOD CONTAMINATION; FOOD MICROBIOLOGY; FUNGI; LACTOBACILLUS; RISK; SPECIES SPECIFICITY;

EID: 84930205022     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2015.04.042     Document Type: Review

References (59)

1. Bhat R., Rai R., Karim A. Mycotoxins in food and feed: present status and future concerns. Compr. Rev. Food Sci. Food Saf. 2010, 9:57-81.
2. Broberg A., Jacobsson K., Ström K., Schnürer J. Metabolite profiles of lactic acid bacteria in grass silage. Appl. Environ. Microbiol. 2007, 73:5547-5552. (Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2042065/pdf/2939-06.pdf. Accessed 05 May 2014).
3. Dalié D., Deschamps A., Richard-Forget F. Lactic acid bacteria - potential for control of mold growth and mycotoxins: a review. Food Control 2010, 21:370-380.
4. Deabes M., Darwish H., Abdel-Aziz K., Farag I., Nada S., Tawfek N. Protective effects of Lactobacillus rhamnosus GG on aflatoxins-induced toxicities in male albino mice. J. Environ. Anal. Toxicol. 2012, 2:132. 10.4172/2161-0525.1000132.
5. Delcour J., Ferain T., Deghorain M., Palumbo E., Hols P. The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie Van Leeuwenhoek 1999, 76:159-184.
6. Di Natale F., Gallo M., Nigro M. Absorbents selection for aflatoxins removal in bovine milks. J. Food Eng. 2009, 95:186-191.
7. El Khoury A., Atoui A., Yaghi J. Analysis of aflatoxin M1 in milk and yogurt and AFM1 reduction by lactic acid bacteria used in Lebanese industry. Food Control 2011, 22:1695-1699.
8. El-Nezami H., Kankaanpää P., Salminen S., Ahokas J. Ability of dairy strains of lactic acid bacteria to bind a common food carcinogen, aflatoxin B1. Food Chem. Toxicol. 1998, 36:321-326.
9. El-Nezami Hani, Kankaanpää P., Salminen S., Ahokas J. Physicochemical alterations enhance the ability of dairy strains of lactic acid bacteria to remove aflatoxin from contaminated media. J. Food Prot. 1998, 61:466-468.
10. El-Nezami H., Mykkänen H., Kankaanpää P., Salminen S., Ahokas J. Ability of Lactobacillus and Propionibacterium strains to remove aflatoxin B1 from the chicken duodenum. J. Food Prot. 2000, 63:549-552.
11. EU Directive 2002/32/EC Available from:, (Accessed 14 August 2014). http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CONSLEG:2002L0032:20061020:EN:PDF.
12. EU Commission regulation (EC) No 1881/2006, setting maximum levels for certain contaminants in foodstuffs Available from:, (Accessed 14 August 2014). http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CONSLEG:2006R1881:20100701:EN:PDF.
13. FAO Worldwide Regulations for Mycotoxins in Food and Feed in 2003: 3. Mycotoxin Regulations in 2003 and Current Developments 2003, (Available from: http://www.fao.org/docrep/007/y5499e/y5499e07.htm. Accessed 26 May 2014).
14. FAO, WHO Report of the Twenty-fourth Session of the Codex Committee in Food Additives and Contaminants 1993, Joint FAO/WHO Food Standards Programme, The Hague, (Available from: http://www.google.co.ke/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&ved=0CCoQFjAA&url=http%3A%2F%2Fwww.codexalimentarius.org%2Finput%2Fdownload%2Freport%2F18%2Fal93_12e.pdf&ei=qrdnUuynLsSUtAbEnYCADw&usg=AFQjCNHn8wXZ0MMZQbFD1rsyTM-M5pDoBw&bvm=bv.55123115,d.Yms. Accessed 23 October 2013).
15. FAO, WHO Report of the Thirtieth Session of the Codex Committee on Food Additives and Contaminants 1999, Joint FAO/WHO Food Standards Programme, Rome, (Available from: http://www.google.co.ke/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&ved=0CC0QFjAA&url=http%3A%2F%2Fwww.codexalimentarius.org%2Finput%2Fdownload%2Freport%2F24%2FAl99_12e.pdf&ei=DbhnUo3ZKYnEswbN04GQCw&usg=AFQjCNHAqVttR_P-BpRU0UfTqn5VdlPTdw&bvm=bv.55123115,d.Yms. Accessed 15 August 2014).
16. Gerbaldo G., Barberis C., Pascual L., Dalcero A., Barberis L. Antifungal activity of two Lactobacillus strains with potential probiotic properties. FEMS Microbiol. Lett. 2012, 332:27-33.
17. Gourama H., Bullerman L.B. Inhibition of growth and aflatoxin production of Aspergillus flavus by Lactobacillus species. J. Food Prot. 1995, 58:1249-1256.
18. Gratz S., Mykkänen H., Ouwehand A.C., Juvonen R., Salminen S., El-Nezami H. Intestinal mucus alters the ability of probiotic bacteria to bind aflatoxin B1 in vitro. Appl. Environ. Microbiol. 2004, 70:1-4.
19. Gratz S., Mykkänen H., El-Nezami H. Aflatoxin B1 binding by a mixture of Lactobacillus and Propionibacterium: in vitro versus ex vivo. J. Food Prot. 2005, 68:2470-2474.
20. Gratz S., Täubel M., Juvonen R.O., Viluksela M., Turner P.C., Mykkänen H., El-Nezami H. Lactobacillus rhamnosus strain GG modulates intestinal absorption, fecal excretion, and toxicity of aflatoxin B1 in rats. Appl. Environ. Microbiol. 2006, 72:7398-7400.
21. Gratz S., Wu Q., El-Nezami H., Juvonen R., Mykkänen H., Turner P.C. Lactobacillus rhamnosus strain GG reduces aflatoxin B1 transport, metabolism, and toxicity in Caco-2 cells. Appl. Environ. Microbiol. 2007, 73:3958-3964.
22. Guengerich F. Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chem. Res. Toxicol. 2001, 14:611-650. (Available from: http://pubs.acs.org/doi/abs/10.1021/tx0002583 Accessed 26 May 2014).
23. Halttunen T., Collado M., El-Nezami H., Meriluoto J., Salminen S. Combining strains of lactic acid bacteria may reduce their toxin and heavy metal removal efficiency from aqueous solution. Lett. Appl. Microbiol. 2008, 46:160-165.
24. Haskard C., Binnion C., Ahokas J. Factors affecting the sequestration of aflatoxin by Lactobacillus rhamnosus strain GG. Chem. Biol. Interact. 2000, 128:39-49.
25. Haskard C., El-Nezami H., Kankaanpää P., Salminen S., Ahokas J. Surface binding of aflatoxin B1 by lactic acid bacteria. Appl. Environ. Microbiol. 2001, 67:3086-3091.
26. Hathout A., Mohamed S., El-Nekeety A., Hassan N., Aly S., Abdel-Wahhab M. Ability of Lactobacillus casei and Lactobacillus reuteri to protect against oxidative stress in rats fed aflatoxins-contaminated diet. Toxicon 2011, 58:179-186.
27. Hernandez-Mendoza A., Garcia H., Steele J. Screening of Lactobacillus casei strains for their ability to bind aflatoxin B1. Food Chem. Toxicol. 2009, 47:1064-1068.
28. Hernandez-Mendoza A., Guzman-de-Peña D., Garcia H.S. Key role of teichoic acids on aflatoxin B1 binding by probiotic bacteria. J. Appl. Microbiol. 2009, 107:395-403.
29. Hernandez-Mendoza A., Guzman-De-Peña D., González-Córdova A.F., Vallejo-Córdoba B., Garcia H.S. In vivo assessment of the potential protective effect of Lactobacillus casei Shirota against aflatoxin B1. Dairy Sci. Technol. 2010, 90:729-740.
30. IARC Volume 82 Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 2002, (Available from: http://monographs.iarc.fr/ENG/Monographs/vol82/mono82.pdf. Accessed 23 October 2013).
31. Ismaiel A., Ghaly M.F., El-Naggar A.K. Milk kefir: ultrastructure, antimicrobial activity and efficacy on aflatoxin B1 production by Aspergillus flavus. Curr. Microbiol. 2011, 62:1602-1609.
32. Kabak B., Ozbey F. Assessment of the bioaccessibility of aflatoxins from various food matrices using an in vitro digestion model, and the efficacy of probiotic bacteria in reducing bioaccessibility. J. Food Compos. Anal. 2012, 27:21-31.
33. Kabak B., Ozbey F. Aflatoxin M1 in UHT milk consumed in Turkey and first assessment of its bioaccessibility using an in vitro digestion model. Food Control 2012, 28:338-344.
34. Kankaanpää P., Tuomola E., El-Nezami H., Ahokas J., Salminen S.J. Binding of aflatoxin B1 alters the adhesion properties of Lactobacillus rhamnosus strain GG in a Caco-2 model. J. Food Prot. 2000, 63:412-414.
35. Kpodo K., Thrane U., Hald B. Fusaria and fumonisins in maize from Ghana and their co-occurrence with aflatoxins. Int. J. Food Microbiol. 2000, 61:147-157.
36. Lahtinen S.J., Haskard C.A., Ouwehand A.C., Salminen S.J., Ahokas J.T. Binding of aflatoxin B1 to cell wall components of Lactobacillus rhamnosus strain GG. Food Addit. Contam. 2004, 21:158-164.
37. Laitila A., Alakomi H.-L., Raaska L., Mattila-Sandholm T., Haikara A. Antifungal activities of two Lactobacillus plantarum strains against Fusarium molds in vitro and in malting of barley. J. Appl. Microbiol. 2002, 93:566-576.
38. Ndagano D., Lamoureux T., Dortu C., Vandermoten S., Thonart P. Antifungal activity of 2 lactic acid bacteria of the Weissella genus isolated from food. J. Food Sci. 2011, 76:305-311.
39. Niderkorn V., Boudra H., Morgavi D. Binding of Fusarium mycotoxins by fermentative bacteria in vitro. J. Appl. Microbiol. 2006, 101:849-856.
40. Oluwafemi F., Da-Silva F.A. Removal of aflatoxins by viable and heat-killed Lactobacillus species isolated from fermented maize. J. Appl. Biosci. 2009, 16:871-876.
41. Oluwafemi F., Kumar M., Bandyopadhyay R., Ogunbanwo T., Ayanwande K.B. Bio-detoxification of aflatoxin B1 in artificially contaminated maize grains using lactic acid bacteria. Toxin Rev. 2010, 29:115-122.
42. Onilude A.A., Fagade O.E., Bello M.M., Fadahunsi I.F. Inhibition of aflatoxin-producing aspergilli by lactic acid bacteria isolates from indigenously fermented cereal gruels. Afr. J. Biotechnol. 2005, 4:1404-1408.
43. Peltonen K.D., El-Nezami H.S., Salminen S.J., Ahokas J.T. Binding of aflatoxin B1 by probiotic bacteria. J. Sci. Food Agric. 2000, 80:1942-1945.
44. Peltonen K., El-Nezami H., Haskard C., Ahokas J., Salminen S. Aflatoxin B1 binding by dairy strains of lactic acid bacteria and bifidobacteria. J. Dairy Sci. 2001, 84:2152-2156.
45. Pierides M., El-Nezami H., Peltonen K., Salminen S., Ahokas J. Ability of dairy strains of lactic acid bacteria to bind aflatoxin M1 in a food model. J. Food Prot. 2000, 63:645-650.
46. Pizzolitto R.P., Salvano M.A., Dalcero A.M. Analysis of fumonisin B1 removal by microorganisms in co-occurrence with aflatoxin B1 and the nature of the binding process. Int. J. Food Microbiol. 2012, 156:214-221.
47. Sarimehmetoğlu B., Küplülü Ö. Binding ability of aflatoxin M1 to yoghurt bacteria. Ank. Univ. Vet. Fak. Derg. 2004, 51:195-198. (Available from: http://dergiler.ankara.edu.tr/dergiler/11/214/1752.pdf. Accessed 14 August 2014).
48. Shahin A. Removal of aflatoxin B1 from contaminated liquid media by dairy lactic acid bacteria. Int. J. Agric. Biol. 2007, 9:71-75.
49. Shetty H.P., Hald B., Jespersen L. Surface binding of aflatoxin B1 by Saccharomyces cerevisiae strains with potential decontaminating abilities in indigenous fermented foods. Int. J. Food Microbiol. 2007, 113:41-46.
50. Strosnider H., Azziz-Baumgartner E., Banziger M., Bhat R.V., Breiman R., Brune M.-N., DeCock K., Dilley A., Groopman J., Hell K., Henry S.H., Jeffers D., Jolly C., Jolly P., Kibata G.N., Lewis L., Liu X., Luber G., McCoy L., Mensah P., Miraglia M., Misore A., Njapau H., Ong C.-N., Onsongo M.T.K., Page W.S., Park D., Patel M., Phillips T., Pineiro M., Pronczuk J., Schurz Rogers H., Rubin C., Sabino M., Schaafsma A., Shephard G., Stroka J., Wild C., Williams J.T., Wilson D. Workgroup report: public health strategies for reducing aflatoxin exposure in developing countries. Environ. Health Perspect. 2006, 114:1898-1903.
51. Turbic A., Ahokas J., Haskard C. Selective in vitro binding of dietary mutagens, individually or in combination, by lactic acid bacteria. Food Addit. Contam. 2002, 19:144-153.
52. Turner P.C., Sylla A., Gong Y.Y., Diallo M.S., Sutcliffe A.E., Hall A.J., Wild C.P. Reduction in exposure to carcinogenic aflatoxins by postharvest intervention measures in west Africa: a community-based intervention study. Lancet 2005, 365:1950-1956.
53. Valerio F., Lavermicocca P., Pascale M., Visconti A. Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol. Lett. 2004, 233:289-295.
54. Valerio F., Favilla M., de Bellis P., Sisto A., de Candia S., Lavermicocca P. Antifungal activity of strains of lactic acid bacteria isolated from a semolina ecosystem against Penicillium roqueforti, Aspergillus niger and Endomyces fibuliger contaminating bakery products. Syst. Appl. Microbiol. 2009, 32:438-448.
55. Vanne L., Kleemola T., Haikara A. Screening of the antifungal effect of lactic acid bacteria against toxigenic Penicillium and Aspergillus strains. BMS International Symposium on Bioactive Fungal Metabolites - Impact and Exploitation 2001, 100. University of Wales Swansea, British Mycological Society.
56. Wu F., Tritscher A. Aflatoxins: a global public health problem Available from:, (Accessed 14 August 2014). http://www.agriskmanagementforum.org/sites/agriskmanagementforum.org/files/WHO%20-%20Aflatoxin-public%20health%20issue.pdf.
57. Wu F., Narrod C., Tiongco M., Liu Y. The health economics of aflatoxin: global burden of disease Available from:, (Accessed 14 August 2014). http://www.ifpri.org/sites/default/files/publications/aflacontrol_wp04.pdf.
58. Yang E., Chang H. Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int. J. Food Microbiol. 2010, 139:56-63.
59. Zinedine A., Faid M., Benlemlih M. In vitro reduction of aflatoxin B1 by strains of lactic acid bacteria isolated from Moroccan sourdough bread. Int. J. Agric. Biol. 2005, 7:67-70.