The Open Microbiology Journal




ISSN: 1874-2858 ― Volume 13, 2019

Antifungal Activity and Aflatoxin Degradation of Bifidobacterium Bifidum and Lactobacillus Fermentum Against Toxigenic Aspergillus Parasiticus



Roshanak Daie Ghazvini1, Ebrahim Kouhsari1, Ensieh Zibafar1, Seyed Jamal Hashemi1, 2, Abolfazl Amini3, Farhad Niknejad3, *
1 Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
2 Food Microbiology Research Center, Tehran University of Medical Sciences, Tehran, Iran
3 Laboratory Sciences Research Center, Golestan University of Medical Sciences, Gorgan, Iran

Abstract

Food and feedstuff contamination with aflatoxins (AFTs) is a serious health problem for humans and animals, especially in developing countries. The present study evaluated antifungal activities of two lactic acid bacteria (LAB) against growth and aflatoxin production of toxigenic Aspergillus parasiticus. The mycelial growth inhibition rate of A. parasiticus PTCC 5286 was investigated in the presence of Bifidobacterium bifidum PTCC 1644 and Lactobacillus fermentum PTCC 1744 by the pour plate method. After seven days incubation in yeast extract sucrose broth at 30°C, the mycelial mass was weighed after drying. The inhibitory activity of LAB metabolites against aflatoxin production by A. parasiticus was evaluated using HPLC method. B. bifidum and L. fermentum significantly reduced aflatoxin production and growth rate of A. parasiticus in comparison with the controls (p≤0.05). LAB reduced total aflatoxins and B1, B2, G1 and G2 fractions by more than 99%. Moreover, LAB metabolites reduced the level of standard AFB1, B2, G1 and G2 from 88.8% to 99.8% (p≤0.05). Based on these findings, B. bifidum and L. fermentum are recommended as suitable biocontrol agents against the growth and aflatoxin production by aflatoxigenic Aspergillus species.

Keywords: Aspergillus parasiticus, Aflatoxin, Antifungal activity, Bifidobacterium bifidum, Lactobacillus fermentum.


Article Information


Identifiers and Pagination:

Year: 2016
Volume: 10
First Page: 197
Last Page: 201
Publisher Id: TOMICROJ-10-197
DOI: 10.2174/1874285801610010197

Article History:

Received Date: 02/11/2015
Revision Received Date: 24/5/2016
Acceptance Date: 26/5/2016
Electronic publication date: 30/11/2016
Collection year: 2016

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© Ghazvini et al.; Licensee Bentham Open.

open-access license: This is an open access article licensed under the terms of the Creative Commons Attribution-Non-Commercial 4.0 International Public License (CC BY-NC 4.0) (https://creativecommons.org/licenses/by-nc/4.0/legalcode), which permits unrestricted, non-commercial use, distribution and reproduction in any medium, provided the work is properly cited.


* Address correspondence to this author at the Laboratory Sciences Research Center, Golestan University of Medical Sciences, Gorgan, Irann; Tel: +98-17-32421664; Fax: +98-17-32423630; E-mail: niknejad@goums.ac.ir




1. INTRODUCTION

The presence of various fungal species such as Aspergillus, Penicillium and Fusarium in food commodities can cause serious health problems in humans and animals, which leads to unfavorable economic effects [1Blagojev N, Skrinjar M, Veskovic-Moracanin S, Soso V. Control of mould growth and mycotoxin production by lactic acid bacteria metabolites. Rom Biotechnol Lett 2012; 17: 7219-26.]. Some toxigenic Aspergillus strains such as A. flavus and A. parasiticus produce aflatoxin, an important carcinogenic mycotoxin with side effects such as malformations and immune suppression [2Delie DK, Deschamps AM, Richard-Forget F. Lactic acid bacteria–Potential for control of mound growth and mycotoxins: A review. J Food Control 2010; 21: 370-80.
[http://dx.doi.org/10.1016/j.foodcont.2009.07.011]
, 3Gourama H, Bullerman LB. Anti aflatoxigenic activity of Lactobacillus casei pseudoplantarum. Int J Food Microbial 1997; 34: 131-34.]. Physical, chemical and biological methods have been developed for degradation of mycotoxins in food. Since the chemical and biological methods are often regarded as unsafe and expensive, it seems that biodegradation of mycotoxins is the best option.

There are several reports on the interactions between toxigenic fungi and microorganisms that can affect fungal growth and toxin production due to antagonist compounds [2Delie DK, Deschamps AM, Richard-Forget F. Lactic acid bacteria–Potential for control of mound growth and mycotoxins: A review. J Food Control 2010; 21: 370-80.
[http://dx.doi.org/10.1016/j.foodcont.2009.07.011]
]. Lactic acid bacteria (LAB) are among these microorganisms and Bifidobacterium and Lactobacillus are two well-known genera of this family [3Gourama H, Bullerman LB. Anti aflatoxigenic activity of Lactobacillus casei pseudoplantarum. Int J Food Microbial 1997; 34: 131-34.]. LAB are found in dairy products, meat and cereal products [4Carr FJ, Chill D, Maida N. The lactic acid bacteria: a literature survey. Crit Rev Microbiol 2002; 28(4): 281-370.
[http://dx.doi.org/10.1080/1040-840291046759] [PMID: 12546196]
]. Several species and subspecies such as Lactococcus lactis, L. cremoris, L. diacetylactis, L. acidophilus, L. plantarum and L. curvatus are able to synthesize antimicrobial peptides or proteins known as bacteriocins [5Batish VK, Roy U, Lal R, Grover S. Antifungal attributes of lactic acid bacteria--a review. Crit Rev Biotechnol 1997; 17(3): 209-25.
[http://dx.doi.org/10.3109/07388559709146614] [PMID: 9306649]
]. LAB have been used for centuries as starter cultures in the food industry and are able to produce different types of bioactive metabolites such as fatty acids, organic acids, aroma compounds, hydrogen peroxide and bacteriocins [6Hassan YI, Bullerman LB. Antifungal activity of Lactobacillus paracasei ssp. tolerans isolated from a sourdough bread culture. Int J Food Microbiol 2008; 121(1): 112-5.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2007.11.038] [PMID: 18077044]
].

In recent years, biopreservation (the use of microorganisms and/or their metabolites to prevent spoilage and to extend the shelf life of foods) has gained a lot of attention because of consumer demand [7Stiles ME. Biopreservation by lactic acid bacteria. Antonie van Leeuwenhoek 1996; 70(2-4): 331-45.
[http://dx.doi.org/10.1007/BF00395940] [PMID: 8879414]
].

The aim of the present study was to evaluate the antifungal activities of B. bifidum and L. fermentum against toxigenic Aspergillus parasiticus.

2. MATERIAL AND METHODS

2.1. Microorganisms and Culture Conditions

Standard strains of B. bifidum PTCC 1644, L. fermentum PTCC 1744, toxigenic A. parasiticus PTCC 5286 and nontoxigenic A. niger (as negative control) were purchased from the Iranian Research Organization for Science and Technology (IROST). A. parasiticus was stored in sterile distilled water at room temperature and then grown on Sabouraud dextrose agar at 30 °C for five days until the start of experiments [8Penna ML, Etcheverry M. Impact on growth and aflatoxin B1 accumulation by Kluyveromyces isolates at different water activity conditions. Mycopathologia 2006; 162(5): 347-53.
[http://dx.doi.org/10.1007/s11046-006-0071-4] [PMID: 17123033]
, 9Niknejad F, Zaini F, Faramarzi M, et al. Candida parapsilosis as a potent biocontrol agent against growth and aflatoxin production by aspergillus species. Iran J Public Health 2012; 41(10): 72-80.
[PMID: 23308351]
].

LAB were separately incubated in tryptic soy broth (Conda laboratories, Madrid, Spain) at 37 °C for 48 h. Grown bacteria were spread on Man-Rogasa-Sharpe agar and allowed to grow at 38°C for 48 h in an anaerobic jar. Standard aflatoxins (AFT) B1, B2, G1 and G2 were purchased from Sigma-Aldrich Chemical Co.

2.2. Effect of Lactic Acid Bacteria on Growth Rate and AFT Production of A. Parasiticus

A loopful of LAB from the Man-Rogasa-Sharpe medium was separately incubated in tryptic soy broth at 37 °C for 18 h. Then, one mL of culture medium (density equivalent to 0.5 MacFarland standard) was added to a 100 mL Erlenmeyer flask containing 25 mL of yeast extract sucrose broth with 5 × 104 spores/mL of A. parasiticus. Mycelial mass and AFT production rates were measured according to the method described previously [1Blagojev N, Skrinjar M, Veskovic-Moracanin S, Soso V. Control of mould growth and mycotoxin production by lactic acid bacteria metabolites. Rom Biotechnol Lett 2012; 17: 7219-26., 10Muñoz R, Arena ME, Silva J, González SN. Inhibition of mycotoxin-producing Aspergillus nomius vsc 23 by lactic acid bacteria and Saccharomyces cerevisiae. Braz J Microbiol 2010; 41(4): 1019-26.
[http://dx.doi.org/10.1590/S1517-83822010000400021] [PMID: 24031582]
, 11Onilude A, Fagade OE, Bello MM, Fadahunsi IF. Inhibition of aflatoxin-producing Aspergilla by lactic acid bacteria isolates from indigenously fermented cereal granules. Afr J Biotechnol 2005; 4: 1404-8.].

Fungal mycelial mass was separated by Filter Paper (Whatman No. 1) and weighed after drying in oven at 70°C. The amount of AFTs in the medium was analyzed by HPLC method. In brief, a volume of 10 mL chloroform was added to 50 mL of culture media supernatant, and then agitated vigorously. After 15 minutes, the supernatant was removed and evaporated with N2 under safety cabinet and reconstituted in 10 mL phosphate buffer saline (pH 7.2), and then passed through a membrane filter (0.45 µM pore size). The filtrate passed through the Immunoaffinity Afla-clean column (LC Tech, Germany) at flow rate of 1 drop/second. The column was washed with 10 mL of deionized water. Finally, AFTs were eluted using methanol through the two following steps: 1 mL methanol was applied to the column and was allowed to pass by gravity after 5 minutes, 1 mL additional methanol was poured into the column after a minute and elute was later collected and 50 µL injected to HPLC. Water/methanol/acetonitrile (60:30:10, v/v/v) were used as the mobile phase with a flow rate of 1.0 mL/min at 25°C [9Niknejad F, Zaini F, Faramarzi M, et al. Candida parapsilosis as a potent biocontrol agent against growth and aflatoxin production by aspergillus species. Iran J Public Health 2012; 41(10): 72-80.
[PMID: 23308351]
]. The retention time was 20 min. A five- point calibration curve was drawn for different types of AFTs to compare and determine linear correlations. All tests were carried out in duplicate for each sample.

2.3. Effect of LAB Extracellular Metabolites on Standard AFTs

The culture medium containing LAB was centrifuged at 4000 g for 15 min to precipitate bacterial cells. Supernatant was filtered using 0.22 μM membrane filter and then 0.25 μL of mixture fraction of AFTs (1000 ppb) was added to 1.75 mL of the filtrated supernatant to reach a final concentration of 125 ppb for AFB1&AFG1 and 25 ppb for AFB2&AFG2. The final solution was incubated at 30°C for 72 h. The amounts of AFTs were analyzed according to the method described previously [9Niknejad F, Zaini F, Faramarzi M, et al. Candida parapsilosis as a potent biocontrol agent against growth and aflatoxin production by aspergillus species. Iran J Public Health 2012; 41(10): 72-80.
[PMID: 23308351]
].

2.4. Statistical Analysis

Statistical analysis was performed using paired-samples T-test by SPSS 21 statistical software. P-value of ≤ 0.05 was considered as the statistical significance level.

3. RESULTS

3.1. Antifungal Activity of LAB Against Growth of A. Parasiticus

Both Bifidobacterium and Lactobacillus significantly reduced the growth rate of A. parasiticus in comparison with the positive control (p<0.05). However, there was no significant difference between the antifungal activities of these two LAB (Table 1).

Table 1
Mycelial mass production by A. parasiticus in the presence of L. fermentum and B. bifidum.


3.2. Impact of LAB on Aflatoxin Production by A. Parasiticus

Both bacteria significantly reduced AFB1, AFB2 and AFG1 production (p ≤ 0.05), while this reduction was not significant in the case of AFG2 (Table 2).

Table 2
Effect of L. fermentum and B. bifidum on the concentration of AFTs produced by toxigenic A. parasiticus.


3.3. Effects of LAB Extracellular Metabolites on AFT Standard Solution

The extracellular metabolites filtrated from both LAB significantly reduced the mixture fractions of AFTs from 88.8% to 99.8% (Table 3).

Table 3
Aflatoxin reduction by extracellular metabolites of L. fermentum and B. bifidum in AFTs mixture solution containing AFB1 and G1= 125 ppb, AFB2 and G2= 25 ppb.


4. DISCUSSION

It has been clear that the best effective way to prevention of food with mycotoxins contamination is to avoid of the growth mycotoxicogenic fungi [1Blagojev N, Skrinjar M, Veskovic-Moracanin S, Soso V. Control of mould growth and mycotoxin production by lactic acid bacteria metabolites. Rom Biotechnol Lett 2012; 17: 7219-26.].

The interaction between mycotoxin–producing fungi and other microorganisms is a suitable biological method to control fungal food poisoning and contamination by blocking the mycotoxins pathway [1Blagojev N, Skrinjar M, Veskovic-Moracanin S, Soso V. Control of mould growth and mycotoxin production by lactic acid bacteria metabolites. Rom Biotechnol Lett 2012; 17: 7219-26., 12Varga JZ, Peteri K, Tabori J, Teren C, Vagvolgy I. Degradation on ochrotoxin A and other mycotoxins by Rhizopus isolates. Int J Food Microbiol 2005; 99: 321-8.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2004.10.034] [PMID: 15808366]
]. In the present study, B. bifidum and L. fermentum caused significant reduction in the mycelial growth of A. parasiticus. In addition, these LAB exhibited inhibitory effects on the standard solution of AFTs from 88.8% to 99.8% in comparison with the control. The results of this study are in agreement with the study of Munoz et al. in which two LAB of L. fermentum and L. rhamnosus, and S. cerevisiae inhibited the growth of mold and mycotoxin–producing A. nomius. However, L. rhamnosus showed the highest fungal inhibitory activity compared with the other bacteria tested [10Muñoz R, Arena ME, Silva J, González SN. Inhibition of mycotoxin-producing Aspergillus nomius vsc 23 by lactic acid bacteria and Saccharomyces cerevisiae. Braz J Microbiol 2010; 41(4): 1019-26.
[http://dx.doi.org/10.1590/S1517-83822010000400021] [PMID: 24031582]
]. The results of the present study are also consistent with the findings of Ghonaimy et al. on the growth inhibition of A. flavus and A. parasiticus and AFT production by L. acidophilus ATCC 4495 and ATCC 20552 [13Ghonaimy GA, Yonis AA, Abol-Ela MF. Inhibition of Aspergillus flavus and A. parasiticus fungal growth and its aflatoxins (B1, B2, G1 and G2) production by Lactobacillus acidophilus. J Egypt Soc Toxicol 2007; 37: 53-60.].

Various factors including nutritional competition, secondary metabolites, pH or their combinations have been proposed for the inhibition of fungal growth by the bacteria [14Magnusson J, Ström K, Roos S, Sjögren J, Schnürer J. Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiol Lett 2003; 219(1): 129-35.
[http://dx.doi.org/10.1016/S0378-1097(02)01207-7] [PMID: 12594034]
, 15El-Nezami H, Polychronaki N, Salminen S, Mykkänen H. Binding rather than metabolism may explain the interaction of two food-Grade Lactobacillus strains with zearalenone and its derivative (’)alpha-earalenol. Appl Environ Microbiol 2002; 68(7): 3545-9.
[http://dx.doi.org/10.1128/AEM.68.7.3545-3549.2002] [PMID: 12089040]
]. El-Nezami et al. investigated the reduction of AFT by five Lactobacillus species and showed that, the binding of AFT with probiotic strains, such as L. rhamnosus GG and L. rhamnosus LC-705 was very effective in removing AFB1 and more than 80% of the toxin trapped [16El-Nezami H, Kankaanpä 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(4): 466-8.
[PMID: 9709211]
].

Piotrowska et al. reported ochratoxin removal from culture media by L. plantarum, L. brevis and L. sanfranciscensis. In the mentioned study, ochratoxin reduction appeared with adsorption to bacterial cell wall with hydrophobic phenomenon, electron donor-acceptor and Lewis acid-base properties and no active metabolites were seen in this process [17Piotrowska M. The adsorption of ochratoxin a by lactobacillus species. Toxins (Basel) 2014; 6(9): 2826-39.
[http://dx.doi.org/10.3390/toxins6092826] [PMID: 25247265]
].

Carbohydrates and/or protein components of LAB cell wall play a major role in the binding of AFT to LAB [18Haskard CA, El-Nezami HS, Kankaanpä PE, Salminen S, Ahokas JT. Surface binding of aflatoxin B(1) by lactic acid bacteria. Appl Environ Microbiol 2001; 67(7): 3086-91.
[http://dx.doi.org/10.1128/AEM.67.7.3086-3091.2001] [PMID: 11425726]
]. Fulgueira et al. in 2004 detected a proteinaceous compound from Streptomyces sp. with high antagonistic activity on toxigenic fungi [19Fulgueira CL, Amigot SL, Magni C. Growth inhibition of toxigenic fungi by a proteinaceous compound from Streptomyces sp. C/33-6. Curr Microbiol 2004; 48(2): 135-9.
[http://dx.doi.org/10.1007/s00284-003-4128-z] [PMID: 15057482]
].

In the present study, LAB extracellular metabolites significantly reduced the standard solution of AFTs. Consistent with these findings, Lindgren et al., Sjogren et al. and Mondal et al. studies showed that antifungal compounds produced by LAB can significantly reduce AFTs [20Lindgren SE, Dobrogosz WJ. Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol Rev 1990; 7(1-2): 149-63.
[http://dx.doi.org/10.1111/j.1574-6968.1990.tb04885.x] [PMID: 2125429]
-22Mandal V, Sen SK, Mandal NC. Detection, isolation and partial characterization of antifungal compound(s) produced by Pediococcus acidilactici LAB 5. Nat Prod Commun 2007; 2: 671-4.]. Moreover, some ex vivo and in vivo studies demonstrated that LAB reduce or retard the uptake of AFB1 in the gastrointestinal tract [23Gratz 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(11): 2470-4.
[PMID: 16300092]
]. Although the biological decontamination and enzymatic degradation of mycotoxins by different microorganisms have been reported [24Styriak I, Conková E. Microbial binding and biodegradation of mycotoxins. Vet Hum Toxicol 2002; 44(6): 358-61.
[PMID: 12458642]
], the toxicity of enzymatic degradation byproducts and undesired effects of fermentation of non-native microorganisms on food quality remain as problems [25Shetty P, Jespersen L. Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontaminating agents. Trends Food Sci Technol 2006; 17: 48-55.
[http://dx.doi.org/10.1016/j.tifs.2005.10.004]
].

CONCLUSION

LAB are naturally associated with many foods and are well recognized for their biopreservative properties. This study shows the ability of B. bifidum and L. fermentum to reduce aflatoxin levels and prevent growth of mycotoxigenic molds through production of several low-molecular-weight antifungal metabolites, binding to the cell wall or combination of acidity and microbial competition. These antifungal LAB can be used in the food industry instead of chemical preservatives to produce organic foods. Furthermore, the excellent properties of LAB may preserve nutritional value of foods and delay spoilage. The future trends are to include beneficial probiotic microorganisms in a process of dietary detoxification of contaminated foods to constitute an approach for the decrease of the availability of aflatoxins in the human nutrition and animal feed. Due to their economic importance for the food industry and their health-related implications as probiotics safety assessment and risk analysis must be considered.

ETHICAL CONSIDERATIONS

All ethical issues (such as informed consent, plagiarism, misconduct, co-authorship, double submission, etc.) were considered carefully.

CONFLICT OF INTEREST

The authors confirm that this article content has no conflict of interest.

ACKNOWLEDGEMENTS

This study was derived from MSc thesis supported by the Tehran University of Medical Sciences.

REFERENCES

[1] Blagojev N, Skrinjar M, Veskovic-Moracanin S, Soso V. Control of mould growth and mycotoxin production by lactic acid bacteria metabolites. Rom Biotechnol Lett 2012; 17: 7219-26.
[2] Delie DK, Deschamps AM, Richard-Forget F. Lactic acid bacteria–Potential for control of mound growth and mycotoxins: A review. J Food Control 2010; 21: 370-80.
[http://dx.doi.org/10.1016/j.foodcont.2009.07.011]
[3] Gourama H, Bullerman LB. Anti aflatoxigenic activity of Lactobacillus casei pseudoplantarum. Int J Food Microbial 1997; 34: 131-34.
[4] Carr FJ, Chill D, Maida N. The lactic acid bacteria: a literature survey. Crit Rev Microbiol 2002; 28(4): 281-370.
[http://dx.doi.org/10.1080/1040-840291046759] [PMID: 12546196]
[5] Batish VK, Roy U, Lal R, Grover S. Antifungal attributes of lactic acid bacteria--a review. Crit Rev Biotechnol 1997; 17(3): 209-25.
[http://dx.doi.org/10.3109/07388559709146614] [PMID: 9306649]
[6] Hassan YI, Bullerman LB. Antifungal activity of Lactobacillus paracasei ssp. tolerans isolated from a sourdough bread culture. Int J Food Microbiol 2008; 121(1): 112-5.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2007.11.038] [PMID: 18077044]
[7] Stiles ME. Biopreservation by lactic acid bacteria. Antonie van Leeuwenhoek 1996; 70(2-4): 331-45.
[http://dx.doi.org/10.1007/BF00395940] [PMID: 8879414]
[8] Penna ML, Etcheverry M. Impact on growth and aflatoxin B1 accumulation by Kluyveromyces isolates at different water activity conditions. Mycopathologia 2006; 162(5): 347-53.
[http://dx.doi.org/10.1007/s11046-006-0071-4] [PMID: 17123033]
[9] Niknejad F, Zaini F, Faramarzi M, et al. Candida parapsilosis as a potent biocontrol agent against growth and aflatoxin production by aspergillus species. Iran J Public Health 2012; 41(10): 72-80.
[PMID: 23308351]
[10] Muñoz R, Arena ME, Silva J, González SN. Inhibition of mycotoxin-producing Aspergillus nomius vsc 23 by lactic acid bacteria and Saccharomyces cerevisiae. Braz J Microbiol 2010; 41(4): 1019-26.
[http://dx.doi.org/10.1590/S1517-83822010000400021] [PMID: 24031582]
[11] Onilude A, Fagade OE, Bello MM, Fadahunsi IF. Inhibition of aflatoxin-producing Aspergilla by lactic acid bacteria isolates from indigenously fermented cereal granules. Afr J Biotechnol 2005; 4: 1404-8.
[12] Varga JZ, Peteri K, Tabori J, Teren C, Vagvolgy I. Degradation on ochrotoxin A and other mycotoxins by Rhizopus isolates. Int J Food Microbiol 2005; 99: 321-8.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2004.10.034] [PMID: 15808366]
[13] Ghonaimy GA, Yonis AA, Abol-Ela MF. Inhibition of Aspergillus flavus and A. parasiticus fungal growth and its aflatoxins (B1, B2, G1 and G2) production by Lactobacillus acidophilus. J Egypt Soc Toxicol 2007; 37: 53-60.
[14] Magnusson J, Ström K, Roos S, Sjögren J, Schnürer J. Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiol Lett 2003; 219(1): 129-35.
[http://dx.doi.org/10.1016/S0378-1097(02)01207-7] [PMID: 12594034]
[15] El-Nezami H, Polychronaki N, Salminen S, Mykkänen H. Binding rather than metabolism may explain the interaction of two food-Grade Lactobacillus strains with zearalenone and its derivative (’)alpha-earalenol. Appl Environ Microbiol 2002; 68(7): 3545-9.
[http://dx.doi.org/10.1128/AEM.68.7.3545-3549.2002] [PMID: 12089040]
[16] El-Nezami H, Kankaanpä 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(4): 466-8.
[PMID: 9709211]
[17] Piotrowska M. The adsorption of ochratoxin a by lactobacillus species. Toxins (Basel) 2014; 6(9): 2826-39.
[http://dx.doi.org/10.3390/toxins6092826] [PMID: 25247265]
[18] Haskard CA, El-Nezami HS, Kankaanpä PE, Salminen S, Ahokas JT. Surface binding of aflatoxin B(1) by lactic acid bacteria. Appl Environ Microbiol 2001; 67(7): 3086-91.
[http://dx.doi.org/10.1128/AEM.67.7.3086-3091.2001] [PMID: 11425726]
[19] Fulgueira CL, Amigot SL, Magni C. Growth inhibition of toxigenic fungi by a proteinaceous compound from Streptomyces sp. C/33-6. Curr Microbiol 2004; 48(2): 135-9.
[http://dx.doi.org/10.1007/s00284-003-4128-z] [PMID: 15057482]
[20] Lindgren SE, Dobrogosz WJ. Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol Rev 1990; 7(1-2): 149-63.
[http://dx.doi.org/10.1111/j.1574-6968.1990.tb04885.x] [PMID: 2125429]
[21] Sjögren J, Magnusson J, Broberg A, Schnürer J, Kenne L. Antifungal 3-hydroxy fatty acids from Lactobacillus plantarum MiLAB 14. Appl Environ Microbiol 2003; 69(12): 7554-7.
[http://dx.doi.org/10.1128/AEM.69.12.7554-7557.2003] [PMID: 14660414]
[22] Mandal V, Sen SK, Mandal NC. Detection, isolation and partial characterization of antifungal compound(s) produced by Pediococcus acidilactici LAB 5. Nat Prod Commun 2007; 2: 671-4.
[23] 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(11): 2470-4.
[PMID: 16300092]
[24] Styriak I, Conková E. Microbial binding and biodegradation of mycotoxins. Vet Hum Toxicol 2002; 44(6): 358-61.
[PMID: 12458642]
[25] Shetty P, Jespersen L. Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontaminating agents. Trends Food Sci Technol 2006; 17: 48-55.
[http://dx.doi.org/10.1016/j.tifs.2005.10.004]

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(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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