Antimutagenic properties of probiotic bacteria and of organic acids

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Abstract

Antimutagenic activities of live and killed cells of 6 strains of Lactobacillus acidophilus and 9 strains of bifidobacteria and of organic acids usually produced by these probiotic bacteria were determined using 8 potent chemical mutagens and promutagens. The mutagens and promutagens used were N-methyl, N′-nitro, N-nitrosoguanidine; 2-nitroflourene; 4-nitro-O-phenylenediamine; 4-nitroquinoline-N-oxide; Aflatoxin-B; 2-amino-3-methyl-3H-imidazoquinoline; 2-amino-1-methyl-6-phenyl-imidazo (4,5-b) pyridine, and 2-amino-3-methyl-9H-pyrido (3,3-6) indole. The mutagenicity of these mutagens and antimutagenic activity of probiotic bacteria against the mutagens were determined according to the Ames TA-100 assay using a mutant of Salmonella typhimurium. Efficiency of bacterial cells in binding or inhibiting these mutagens was also investigated. Live cells of probiotic bacteria showed higher antimutagenic activity and their efficiency in inhibiting the mutagens was better than killed bacterial cells. Live bacterial cells bound or inhibited the mutagens permanently, whereas killed bacteria released mutagens upon extraction with dimethyl sulfoxide. Among the organic acids, butyric acid showed highest inhibition of mutagens followed by acetic acid. Lactic and pyruvic acids did not show appreciable levels of inhibition.

Introduction

Studies 1, 2have reported the presence of mutagenic compounds in broiled fish and meat. A correlation between regular consumption of high heat cooked food such as fried meat and increased incidence of colorectal cancer has been reported [3]. Zeiger [4]reported a high degree of correlation between in vitro mutagenicity and in vivo carcinogenicity. Presence of mutagens can cause irrecoverable damage to DNA which could lead to carcinogenic conditions. Probiotic microorganisms are defined as `the beneficial microbes which improve the health of consumers when ingested live in sufficient numbers' [5]. When the equilibrium of microflora in the intestine is disturbed, harmful organisms such as Escherichia coli and Bacteroides increase their numbers and toxic chemicals and harmful enzymes are produced by these bacteria. Most of the probiotic strains are natural inhabitants of the intestine of humans and animals. Probiotic bacteria such as Lactobacillus acidophilus and Bifidobacterium spp. and their products of fermentation are claimed to provide antimutagenic and anticarcinogenic properties 6, 7, 8. Antimutagenic activity of fermented milks has been shown against a range of mutagens and promutagens in various test systems based on microbial and mammalian cells 9, 10, 11, 12, 13, 14. Consumption of fermented milk is reported to inhibit the growth of certain types of tumours in mice and rats 15, 16, 17, 18. Oral supplementation of L. acidophilus in humans reduced activities of faecal bacterial enzymes such as β-glucuronidase, nitroreductase and azoreductase that activate procarcinogen into carcinogen and excretion of mutagens in faeces and urine [19]. Peters et al. [20]reported that yogurt was found to be protective against colon cancer.

The mechanism of antimutagenic activities of fermented dairy products or probiotic bacteria has not been clearly understood [21]. Binding of mutagens to microbial cells has been suggested to be a possible mechanism of antimutagenicity [22].

Acetate, propionate and butyrate are the major products of microbial fermentation of dietary fibre and other polysaccharides such as amylose and amylopectin in the human colon 23, 24. Butyrate, a major source of energy for colonic epithelial cells 25, 26, 27, caused differentiation of mammalian and carcinoma cells at low concentration 28, 29.

The objectives of this study were: (i) to evaluate antimutagenic activity of 6 strains of L. acidophilus and 9 strains of Bifidobacterium spp. against 8 potent mutagens and promutagens, (ii) to determine the mechanism of antimutagenic activity of probiotic bacteria, (iii) to evaluate antimutagenic potential of killed cells of probiotic bacteria, and (iv) to determine the antimutagenic activity of organic acids usually produced by probiotic bacteria.

Section snippets

Bacterial strains

Six strains of Lactobacillus acidophilus and 9 strains of bifidobacteria were obtained from the Division of Food Science and Technology, Commonwealth Scientific and Industrial Research Organisation (CSIRO), Highett, Victoria, Australia. Strains of L. acidophilus included 2400, 2401, 2404, 2405, 2409 and 2415 and of bifidobacteria were B. bifidum 1900, 1901, B. infantis 1912, B. adolescentis 1920, B. breve 1930 and B. longum 1941. All strain numbers containing four digits have CSCC (CSIRO

Antimutagenicity of live and killed bacterial cells

The antimutagenic activity of live or killed cells of L. acidophilus strains 2400, 2401, 2404, 2405, 2409 and 2415 against mutagens MNNG, NF, NPD, NQO, AFTB, AMIQ, AMPIP and AMPI is shown in Fig. 1. In general, the live bacterial cells always showed higher antimutagenicity against the mutagens studied. The live cells of L. acidophilus 2400 showed >50% antimutagenicity against 6 of the 8 mutagens and promutagens. L. acidophilus strains 2401, 2404, 2405 and 2409 showed similar patterns of

Conclusions

Strains of probiotic bacteria showed different levels of antimutagenic activity and inhibition of mutagens and promutagens. Generally, most strains of L. acidophilus and bifidobacteria were effective in inhibiting NF (nitrofluorene), NDP (4-nitro-O-phenylenediamine), and AFTB (aflatoxin-B). Similarly, most strains of bifidobacteria showed antimutagenic activity against AMIQ (2-amino-3-methyl-3H-imidazoquinoline).

Live probiotic bacteria exhibited higher antimutagenic activity by inhibiting the

References (35)

  • T. Sujimura, M. Nagao, T. Kawachi, M. Honda, T. Yahagi, Y. Seino, M. Sato, M. Matsukura, T. Matsushima, A. Shirai, M....
  • B Commoner et al.

    Formation of mutagens in beef and beef extract during cooking

    Science

    (1978)
  • G Steineck et al.

    The epidemiological evidence concerning intake of mutagenic activity from the fried surface and the risk of cancer can not justify preventive measures

    Eur. J. Cancer Prev.

    (1993)
  • E Zeiger

    Carcinogenicity of mutagens: predictive capability of the Salmonella mutagenesis assay for rodent carcinogenicity

    Cancer Res.

    (1987)
  • R Fuller

    Probiotics in man and animals

    J. Appl. Bacteriol.

    (1989)
  • C.F Fernandes et al.

    Therapeutic role of dietary lactobacilli and lactobacillic fermented dairy products

    Fed. Eur. Microbiol. Soc. Microbiol. Rev.

    (1987)
  • S.E Gilliland

    Health and nutritional benefits from lactic acid bacteria

    Fed. Eur. Microbiol. Soc. Microbial. Rev.

    (1991)
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