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Ability of probiotic Lactobacillus casei DN 114001 to bind or/and metabolise heterocyclic aromatic amines in vitro

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Abstract

Introduction

Heterocyclic aromatic amines (HCA) are compounds with high mutagenic potential, formed when meat is cooked at high temperatures of 150–300 °C. These compounds contribute to development of colon and gastric cancer. Western diet provides a lot of HCA and influences the available substrates for the intestinal microbiota which can activate HCA to direct acting mutagens. On the other hand, lactic acid bacteria existing in the colon and ingested with food including probiotics, may exert an anti-carcinogenic action, but the mechanism is still poorly understood.

Materials and methods

In the present study we determined the ability of probiotic Lactobacillus casei DN 114001 (Actimel strain) to metabolise or adsorb three HCA: IQ, MelQx and PhIP in vitro. Lactobacilli were cultivated in MRS and in a modified MRS broth with reduced concentrations of nitrogen and carbon (MRS NC), with addition of 25 μg/ml of IQ, MelQx or PhIP. Their concentration after cultivation with L. casei DN 114001 was measured with high-performance liquid chromatography and the genotoxicity was evaluated by the alkaline comet assay.

Results and conclusions

It was measured, that after 24 h cultivation in MRS (cell density was 109 cfu/ml), rapid decrease of IQ and PhIP (98–99%) was observed, and the peaks on chromatograms were almost completely reduced. In case of MeIQx the decrease was about 27%. In a modified MRS broth (cell density was 108 cfu/ml), the ability to decrease HCA concentration during prolonged cultivation (to 168 h) depended on the growth phase of bacteria, and it was about 51.5% for IQ and at about 11.2% for MeIQx. Non-growing cells (in phosphate buffer), could reduce the content of IQ and PhIP from 72 h to the end of incubation. L. casei DN 114001 reduced genotoxicity of HCA (IQ from 46 to 48%; MeIQx from 35 to 65% and PhIP from 32 to 81%), and the degree depended on the incubation time, cell growth and the medium used. It may suggest that bacteria can metabolise or adsorb HCA.

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References

  1. Blasiak J, Kowalik J (2000) A comparison of the in vitro genotoxicity of tri- and hexavalent chromium. Mutat Res 649:135–145

    Google Scholar 

  2. Blaut M, Marteau P, Miller GD, Antoine JM (2006) Probiotics and the intestinal microflora: what impact on the immune system, infections and aging? Curr Nutr Food Sci 2:79–95

    Article  CAS  Google Scholar 

  3. Blaut M, Clavel T (2007) Metabolic diversity of the intestinal microbiota: implications for health and disease. J Nutr 137:S751–S755

    Google Scholar 

  4. Bolognani F, Rumney CJ, Rowland IR (1997) Influence of carcinogen binding by lactic acid-producing bacteria on tissue distribution and in vivo mutagenicity of dietary carcinogens. Food Chem Toxicol 35:535–545

    Article  CAS  Google Scholar 

  5. Burns AJ, Rowland IR (2000) Anti-carcinogenicity of probiotics and prebiotics. Curr Issues Intest Microbiol 1:13–24

    CAS  Google Scholar 

  6. Commane D, Hughes R, Shortt C, Rowland IR (2005) The potential mechanisms involved in the anti-carcinogenic action of probiotics. Mutat Res 591:276–289

    CAS  Google Scholar 

  7. Cummings JH, Antoine JM, Azpiroz F, Bourdet-Sicard R, Brandtzaeg P, Calder PC, Gibson GR, Guarner F, Isolauri E et al (2004) PASSCLAIM: gut health and immunity. Eur J Nutr 43(2S):118S–173S

    Google Scholar 

  8. de Kok TMCM, van Maanen JMS (2000) Evaluation of faecal mutagenicity and colorectal cancer risk. Mutat Res 463:53–101

    Article  Google Scholar 

  9. Egert M, de Graaf AA, Smidt H, de Vos WM, Venema K (2006) Beyond diversity: functional microbiomics of the human colon. Trends Microbiol 14:86–91

    Article  CAS  Google Scholar 

  10. Felton JS, Knize MG, Wu RW, Colvin ME, Hatch FT, Malfatti MA (2007) Mutagenic potency of food-derived heterocyclic amines. Mutat Res 616:90–94

    CAS  Google Scholar 

  11. Gutiérrez C, Marco A, Nogales A, Tebar R (2002) Total and segmental colonic transit time and anorectal manometry in children with chronic idiopathic constipation. J Pediatr Gastroenterol Nutr 35:31–38

    Article  Google Scholar 

  12. Harrison JD, Fell TP, Phipps AW, Smith TJ, Ellender M, Ham GJ, Hodgson A, Wilkins BT (2005) Health implications of dounreay fuel fragment: estimates of doses and risks. www.sepa.org.uk/radioactivity

  13. Humbolt C, Combourieu B, Väisänen ML, Furet JP, Delort AM, Rabot S (2005) 1H nuclear magnetic resonance spectroscopy-based studies of the metabolism of food-borne carcinogen 2-amino-3-methylimidazo[4, 5-f]quinoline by human intestinal microbiota. Appl Environ Microbiol 71:5116–5123

    Article  Google Scholar 

  14. Husni-Hag-Ali R, Gomez-Rodriguez BJ, Mendoza Olivares FJ, Garcia Montes JM, Sachez-Gey Venegas S, Herrerias Gutierrez JM (2003) Measuring colonic transit time in chronic idiopathic constipation. Rev Esp Enferm Dig 95:186–190

    CAS  Google Scholar 

  15. Isolauri E (2004) Probiotics. Best Pract Res Clin Gastroenterol 18:299–313

    Article  Google Scholar 

  16. Kassie F, Lhoste EF, Bruneau A, Zsivkovits M, Ferk F, Uhl M, Zidek T, Knasmuller S (2004) Effect of intestinal microflora from vegetarians and meat eaters on the genotoxicity of 2-amino-3-methylimidazo[4, 5-f]quinoline, a carcinogenic heterocyclic amine. J Chromatogr B 802:211–215

    Article  CAS  Google Scholar 

  17. Keating GA, Layton DW, Felton J (1999) Factors determining dietary intakes of heterocyclic aromatic amines in cooked foods. Mutat Res 443:149–156

    CAS  Google Scholar 

  18. Klaude M, Eriksson S, Nygren J, Ahnstrom G (1996) The comet assay: mechanisms and technical consideration. Mutat Res 363:89–96

    Google Scholar 

  19. Kobayashi M, Hanaoka T, Tsugane S (2007) Validity of a self-administrated food frequency questionnaire in the assessment of heterocyclic amine intake using 2-amino-1-methyl1–6-phenylimidazo[4, 5-b]pyridine (PhIP) levels in hair. Mutat Res 630:14–19

    CAS  Google Scholar 

  20. Lankaputhra WEV, Shah NP (1998) Antimutagenic properties of probiotic bacteria and of organic acids. Mutat Res 397:169–182

    CAS  Google Scholar 

  21. Layton DW, Bogen KT, Knize MG, Hatch FT, Johnson VM, Felton JS (1995) Cancer risk of heterocyclic amines in cooked foods: an analysis and implications for research. Carcinogenesis 16(1):39–52

    Article  CAS  Google Scholar 

  22. Limdi JK, O’Neill C, McLaughlin J (2006) Do probiotics have a therapeutic role in gastroenterology? World J Gastroenterol 12(34):5447–5457

    Google Scholar 

  23. Murkovic M (2007) Analysis of heterocyclic aromatic amines. Anal Bioanal Chem (in press). doi: 10.1007/s00216-007-1306-z

  24. Nakagama H, Ochiai M, Ubagai T, Tajima R, Fujiwara K, Sugimura T, Nagao M (2002) A rat colon cancer model induced by 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine, PhIP. Mutat Res 506–507:137–144

    Google Scholar 

  25. Oba S, Shimizu N, Nagata C, Shimizu H, Kametani M, Takeyama N, Ohnuma T, Matsushita S (2006) The relationship between the consumption of meat, fat, coffee and risk of colon cancer: a perspective study in Japan. Cancer Lett 244:260–267

    Article  CAS  Google Scholar 

  26. O’Keefe SJD, Chung D, Mahmound N, Sepulveda AR, Manafe M, Arch J, Adada H, ban der Melve T (2007) Why do African Americans get more colon cancer than native Africans? J Nutr 137:175S–182S

    Google Scholar 

  27. O’Hara AM, Shanahan F (2007) Gut microbiota: mining for therapeutic potential. Clin Gastroenterol Hepatol 5:274–284

    Article  Google Scholar 

  28. Orrhage K, Sillerstrom E, Gustafsson JA, Nord CE, Rafter J (1994) Binding of heterocyclic amines by intestinal and lactic acid bacteria. Mutat Res 1:239–248

    Google Scholar 

  29. Salmon CP, Knize MG, Felton JS, Zhao B, Seow A (2006) Heterocyclic aromatic amines in domestically prepared chicken and fish from Singapore Chinese households. Food Chem Toxicol 44:484–492

    Article  CAS  Google Scholar 

  30. Shin A, Shrubsole MJ, Ness RM, Wu H, Sinha R, Smalley WE, Shyr Y, Zheng W (2007) Meat and meat-mutagen intake, doneness preference and the risk of colorectal polyps: the Tennessee Colorectal Polyp Study. Int J Cancer 121:136–142

    Article  CAS  Google Scholar 

  31. Sinha R, Rothman N, Salmon CP, Knize MG, Brown ED, Swanson CA, Rhodes D, Rossi S, Felton JS, Levander OA (1998) Heterocyclic amines content in beef cooked by different methods to varying degrees of doneness and gravy made from meat drippings. Food Chem Toxicol 36:279–287

    Article  CAS  Google Scholar 

  32. Singh NP, McCoy M, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

    Article  CAS  Google Scholar 

  33. Sreekumar O, Hosono A (1998) The heterocyclic amine binding receptors of Lactobacillus gasseri cells. Mutat Res 421:65–72

    CAS  Google Scholar 

  34. Terahara M, Meguro S, Kaneko T (1998) Effects of lactic acid bacteria on binding and absorption of mutagenic heterocyclic amines. Biosci Biotechnol Biochem 62:197–200

    Article  CAS  Google Scholar 

  35. Terry PD, Lagergren J, Wolk A, Steineck G, Nyren O, Rothman N (2003) Dietary intake of heterocyclic amines and cancers of the oesophagus and gastric cardia. J Womens Health 12:173–182

    Article  Google Scholar 

  36. Toribio F, Busquets R, Puignou L, Galceran MT (2007) Heterocyclic aromatic amines in griddled beef steak analysed using a single extract clean-up procedure. Food Chem Toxicol 45:667–675

    Article  CAS  Google Scholar 

  37. Turesky RJ (2007) Formation and biochemistry of carcinogenic heterocyclic aromatic amines in cooked meats. Toxicol Lett 168:219–227

    Article  CAS  Google Scholar 

  38. Vanhaecke L, Verstraete W, Van de Wiele T (2006) Metabolism of the food associated carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine by human intestinal microbiota. Reprod Nutr Dev 46(1S):S1–S138

    Google Scholar 

  39. Vanhaecke L, Van Hoof N, Van Brabandt W, Soenen B, Heyerick A, De Kimpe N, De Keukeleire D, Verstraete W, Van de Wiele T (2006) Metabolism of the food associated carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5-b]pyridine by human intestinal microbiota. J Agric Food Chem 54:3454–3461

    Article  CAS  Google Scholar 

  40. Van Tassell RL, Kingston DGI, Wilkins TD (1990) Metabolism of dietary genotoxins by the human colonic microflora: the fecapentaenes and heterocyclic amines. Mutat Res 238:209–221

    Google Scholar 

  41. Wu K, Giovannucci E, Byrne C, Platz EA, Fuchs C, Willett WC, Sinha R (2006) Meat mutagens and risk of distal colon adenoma in cohort of U.S. men. Cancer Epidemiol Biomarkers Prev 15:1120–1125

    Article  CAS  Google Scholar 

  42. Yang CC, Jenq SN, Lee H (1998) Characterization of the carcinogen 2-amino-3, 8-dimethylimidazo[4, 5-f]quinoxaline in cooking aerosols under domestic conditions. Carcinogenesis 19:359–363

    Article  CAS  Google Scholar 

  43. Zhang XB, Ohta Y (1993) Antimutagenicity of cell fractions of microorganisms on potent mutagenic pyrolysates. Mutat Res 298:247–253

    Article  CAS  Google Scholar 

  44. Zoetendal EG, Vaughan EE, de Vos WM (2006) A microbial world within us. Mol Microbiol 59:1639–1650

    Article  CAS  Google Scholar 

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Acknowledgment

The comet assay was conducted with the help of Professor Janusz Blasiak from the Department of Molecular Genetics at the University of Lodz in Poland.

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  1. Institute of Fermentation Technology and Microbiology, Technical University of Lodz, Wolczanska 171/173, 90-924, Lodz, Poland

    Adriana Nowak & Zdzislawa Libudzisz

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  2. Zdzislawa Libudzisz
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Correspondence to Adriana Nowak.

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Nowak, A., Libudzisz, Z. Ability of probiotic Lactobacillus casei DN 114001 to bind or/and metabolise heterocyclic aromatic amines in vitro. Eur J Nutr 48, 419–427 (2009). https://doi.org/10.1007/s00394-009-0030-1

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  • DOI: https://doi.org/10.1007/s00394-009-0030-1

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