In vitro fermentation of nuts results in the formation of butyrate and c9,t11 conjugated linoleic acid as chemopreventive metabolites

European Journal of Nutrition

Volumn 55, Issue 6, 2016, Pages 2063-2073

  Schlormann W ^a   Birringer, M ^b   Lochner, A ^a   Lorkowski, S ^a,c   Richter, I ^b   Rohrer, C ^a,c   Glei, M ^a,c  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b UNIVERSITY OF APPLIED SCIENCES   (Germany)

^c Halle Jena Leipzig ^*  (Germany)

Author keywords

Colon cancer; Conjugated fatty acids; Dietary fiber; In vitro fermentation; Nuts; trans fatty acids

Indexed keywords

BILE ACID; BUTYRIC ACID; CONJUGATED LINOLEIC ACID; DEOXYCHOLIC ACID; FATTY ACID ESTER; MALONALDEHYDE; SHORT CHAIN FATTY ACID; VACCENIC ACID; 11-OCTADECENOIC ACID; BUTYRIC ACID DERIVATIVE; OLEIC ACID; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNSATURATED FATTY ACID;

ALMOND; ARTICLE; FECES MICROFLORA; FERMENTATION; GAS CHROMATOGRAPHY; HAZELNUT; HUMAN; IN VITRO STUDY; LIPID PEROXIDATION; MACADAMIA; PHOTOMETRY; PISTACHIO; SUPERNATANT; WALNUT; CHEMISTRY; COLONIC NEOPLASMS; FECES; INTESTINE FLORA; METABOLISM; MICROBIOLOGY; NUT; PH; PISTACIA;

BILE ACIDS AND SALTS; BUTYRATES; COLONIC NEOPLASMS; CORYLUS; FATTY ACIDS, UNSATURATED; FECES; FERMENTATION; GASTROINTESTINAL MICROBIOME; HUMANS; HYDROGEN-ION CONCENTRATION; JUGLANS; LINOLEIC ACIDS, CONJUGATED; MACADAMIA; MALONDIALDEHYDE; NUTS; OLEIC ACIDS; PISTACIA; PRUNUS DULCIS; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84939550738     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-015-1020-0     Document Type: Article

References (61)

1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:359–386
2. Taylor DP, Burt RW, Williams MS, Haug PJ, Cannon-Albright LA (2010) Population-based family history-specific risks for colorectal cancer: a constellation approach. Gastroenterology 138:877–885
3. Hisamuddin IM, Yang VW (2004) Genetics of colorectal cancer. Med Gen Med 6:13
4. Slattery ML (2000) Diet, lifestyle, and colon cancer. Semin Gastrointest Dis 11:142–146
5. Jacobs ET, Thompson PA, Martinez ME (2007) Diet, gender, and colorectal neoplasia. J Clin Gastroenterol 41:731–746
6. Murphy N, Norat T, Ferrari P, Jenab M, Bueno-de-Mesquita B, Skeie G, Dahm CC, Overvad K, Olsen A, Tjonneland A, Clavel-Chapelon F, Boutron-Ruault MC, Racine A, Kaaks R, Teucher B, Boeing H, Bergmann MM, Trichopoulou A, Trichopoulos D, Lagiou P, Palli D, Pala V, Panico S, Tumino R, Vineis P, Siersema P, van Duijnhoven F, Peeters PH, Hjartaker A, Engeset D, Gonzalez CA, Sanchez MJ, Dorronsoro M, Navarro C, Ardanaz E, Quiros JR, Sonestedt E, Ericson U, Nilsson L, Palmqvist R, Khaw KT, Wareham N, Key TJ, Crowe FL, Fedirko V, Wark PA, Chuang SC, Riboli E (2012) Dietary fibre intake and risks of cancers of the colon and rectum in the European prospective investigation into cancer and nutrition (EPIC). PLoS ONE 7:e39361. doi:10.1371/journal.pone.0039361
7. Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17:259–275
8. Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA (2002) The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 132:1012–1017
9. Ros E (2010) Health benefits of nut consumption. Nutrients 2:652–682
10. Gray J (2006) Dietary Fiber-definition, analysis, physiology and health. ILSI Europe`s Concise Monographs and Report Series. ILSI Europe a.i.s.b.l, Brussels, Belgium
11. Jenab M, Ferrari P, Slimani N, Norat T, Casagrande C, Overad K, Olsen A, Stripp C, Tjonneland A, Boutron-Ruault MC, Clavel-Chapelon F, Kesse E, Nieters A, Bergmann M, Boeing H, Naska A, Trichopoulou A, Palli D, Krogh V, Celentano E, Tumino R, Sacerdote C, Bueno-de-Mesquita HB, Ocke MC, Peeters PH, Engeset D, Quiros JR, Gonzalez CA, Martinez C, Chirlaque MD, Ardanaz E, Dorronsoro M, Wallstrom P, Palmqvist R, van Guelpen B, Bingham S, San Joaquin MA, Saracci R, Kaaks R, Riboli E (2004) Association of nut and seed intake with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biomarkers Prev 13:1595–1603
12. Yang M, Hu FB, Giovannucci EL, Stampfer MJ, Willett WC, Fuchs CS, Wu K, Bao Y (2015) Nut consumption and risk of colorectal cancer in women. Eur J Clin Nutr. doi:10.1038/ejcn.2015.66
13. Schlörmann W, Birringer M, Bohm V, Lober K, Jahreis G, Lorkowski S, Muller AK, Schone F, Glei M (2015) Influence of roasting conditions on health-related compounds in different nuts. Food Chem 180:77–85
14. Gebauer SK, Chardigny JM, Jakobsen MU, Lamarche B, Lock AL, Proctor SD, Baer DJ (2011) Effects of ruminant trans fatty acids on cardiovascular disease and cancer: a comprehensive review of epidemiological, clinical, and mechanistic studies. Adv Nutr 2:332–354
15. Kato I, Majumdar AP, Land SJ, Barnholtz-Sloan JS, Severson RK (2010) Dietary fatty acids, luminal modifiers, and risk of colorectal cancer. Int J Cancer 127:942–951
16. Kuriki K, Wakai K, Hirose K, Matsuo K, Ito H, Suzuki T, Saito T, Kanemitsu Y, Hirai T, Kato T, Tatematsu M, Tajima K (2006) Risk of colorectal cancer is linked to erythrocyte compositions of fatty acids as biomarkers for dietary intakes of fish, fat, and fatty acids. Cancer Epidemiol Biomarkers Prev 15:1791–1798
17. Schwab U, Lauritzen L, Tholstrup T, Haldorssoni T, Riserus U, Uusitupa M, Becker W (2014) Effect of the amount and type of dietary fat on cardiometabolic risk factors and risk of developing type 2 diabetes, cardiovascular diseases, and cancer: a systematic review. Food Nutr Res 58:25145. doi:10.3402/fnr.v58.25145
18. Kuhnt K, Kraft J, Moeckel P, Jahreis G (2006) Trans-11-18:1 is effectively Delta9-desaturated compared with trans-12-18: 1 in humans. Br J Nutr 95:752–761
19. Degen C, Ecker J, Piegholdt S, Liebisch G, Schmitz G, Jahreis G (2011) Metabolic and growth inhibitory effects of conjugated fatty acids in the cell line HT-29 with special regard to the conversion of t11, t13-CLA. Biochim Biophys Acta 1811:1070–1080
20. Palombo JD, Ganguly A, Bistrian BR, Menard MP (2002) The antiproliferative effects of biologically active isomers of conjugated linoleic acid on human colorectal and prostatic cancer cells. Cancer Lett 177:163–172
21. Degen C, Habermann N, Piegholdt S, Glei M, Jahreis G (2012) Human colon cell culture models of different transformation stages to assess conjugated linoleic acid and conjugated linolenic acid metabolism: challenges and chances. Toxicol In Vitro 26:985–992
22. Lux S, Scharlau D, Schlörmann W, Birringer M, Glei M (2012) In vitro fermented nuts exhibit chemopreventive effects in HT29 colon cancer cells. Br J Nutr 108:1177–1186
23. Schlörmann W, Hiller B, Jahns F, Zoger R, Hennemeier I, Wilhelm A, Lindhauer MG, Glei M (2012) Chemopreventive effects of in vitro digested and fermented bread in human colon cells. Eur J Nutr 51:827–839
24. Stein K, Borowicki A, Scharlau D, Scheu K, Brenner-Weiss G, Obst U, Hollmann J, Lindhauer M, Wachter N, Glei M (2011) Modification of an in vitro model simulating the whole digestive process to investigate cellular endpoints of chemoprevention. Br J Nutr 105:678–687
25. Klein A, Friedrich U, Vogelsang H, Jahreis G (2008) Lactobacillus acidophilus 74-2 and Bifidobacterium animalis subsp lactis DGCC 420 modulate unspecific cellular immune response in healthy adults. Eur J Clin Nutr 62:584–593
26. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
27. Keller S, Jahreis G (2004) Determination of underivatised sterols and bile acid trimethyl silyl ether methyl esters by gas chromatography–mass spectrometry-single ion monitoring in faeces. J Chromatogr B Analyt Technol Biomed Life Sci 813:199–207
28. Papastergiadis A, Mubiru E, Van Langenhove H, De MB (2012) Malondialdehyde measurement in oxidized foods: evaluation of the spectrophotometric thiobarbituric acid reactive substances (TBARS) test in various foods. J Agric Food Chem 60:9589–9594
29. Fischer S, Glei M (2013) Health-potential of nuts. Ernaehrungs Umsch Int 60:206–215. doi:10.4455/eu.2013.040
30. Ros E (2009) Nuts and novel biomarkers of cardiovascular disease. Am J Clin Nutr 89:1649S–1656S
31. Borowicki A, Stein K, Scharlau D, Scheu K, Brenner-Weiss G, Obst U, Hollmann J, Lindhauer M, Wachter N, Glei M (2010) Fermented wheat aleurone inhibits growth and induces apoptosis in human HT29 colon adenocarcinoma cells. Br J Nutr 103:360–369
32. Glei M, Hofmann T, Kuster K, Hollmann J, Lindhauer MG, Pool-Zobel BL (2006) Both wheat (Triticum aestivum) bran arabinoxylans and gut flora-mediated fermentation products protect human colon cells from genotoxic activities of 4-hydroxynonenal and hydrogen peroxide. J Agric Food Chem 54:2088–2095
33. Scharlau D, Borowicki A, Habermann N, Hofmann T, Klenow S, Miene C, Munjal U, Stein K, Glei M (2009) Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutat Res 682:39–53
34. Mandalari G, Nueno-Palop C, Bisignano G, Wickham MS, Narbad A (2008) Potential prebiotic properties of almond (Amygdalus communis L.) seeds. Appl Environ Microbiol 74:4264–4270
35. Kepler CR, Hirons KP, McNeill JJ, Tove SB (1966) Intermediates and products of the biohydrogenation of linoleic acid by Butyrinvibrio fibrisolvens. J Biol Chem 241:1350–1354
36. Palmquist DL, Lock AL, Shingfield KJ, Bauman DE (2005) Biosynthesis of conjugated linoleic acid in ruminants and humans. Adv Food Nutr Res 50:179–217
37. Coakley M, Johnson MC, McGrath E, Rahman S, Ross RP, Fitzgerald GF, Devery R, Stanton C (2006) Intestinal bifidobacteria that produce trans-9, trans-11 conjugated linoleic acid: a fatty acid with antiproliferative activity against human colon SW480 and HT-29 cancer cells. Nutr Cancer 56:95–102
38. Ogawa J, Kishino S, Ando A, Sugimoto S, Mihara K, Shimizu S (2005) Production of conjugated fatty acids by lactic acid bacteria. J Biosci Bioeng 100:355–364
39. Chin SF, Storkson JM, Albright KJ, Pariza MW (1994) Conjugated linoleic-acid (9,11-octadecadienoic and 10,12-octadecadienoic acid) is produced in conventional but not germ-free rats fed linoleic-acid. J Nutr 124:694–701
40. Pierre AS, Minville-Walz M, Fevre C, Hichami A, Gresti J, Pichon L, Bellenger S, Bellenger J, Ghiringhelli F, Narce M, Rialland M (2013) Trans-10, cis-12 conjugated linoleic acid induced cell death in human colon cancer cells through reactive oxygen species-mediated ER stress. Biochim Biophys Acta 1831:759–768
41. Bozzo F, Bocca C, Colombatto S, Miglietta A (2007) Antiproliferative effect of conjugated linoleic acid in caco-2 cells: involvement of PPARgamma and APC/beta-catenin pathways. Chem Biol Interact 169:110–121
42. Cho HJ, Kim WK, Jung JI, Kim EJ, Lim SS, Kwon DY, Park JH (2005) Trans-10, cis-12, not cis-9, trans-11, conjugated linoleic acid decreases ErbB3 expression in HT-29 human colon cancer cells. World J Gastroenterol 11:5142–5150
43. Kamlage B, Hartmann L, Gruhl B, Blaut M (1999) Intestinal microorganisms do not supply associated gnotobiotic rats with conjugated linoleic acid. J Nutr 129:2212–2217
44. Herbel BK, McGuire MK, McGuire MA, Shultz TD (1998) Safflower oil consumption does not increase plasma conjugated linoleic acid concentrations in humans. Am J Clin Nutr 67:332–337
45. Abdelmagid SA, Clarke SE, Wong J, Roke K, Nielsen D, Badawi A, El-Sohemy A, Mutch DM, Ma DWL (2013) Plasma concentration of cis9trans11 CLA in males and females is influenced by SCD1 genetic variations and hormonal contraceptives: a cross-sectional study. Nutr Metab 10:1–9
46. Tong JL, Ran ZH, Shen J, Fan GQ, Xiao SD (2008) Association between fecal bile acids and colorectal cancer: a meta-analysis of observational studies. Yonsei Med J 49:792–803
47. Zampa A, Silvi S, Fabiani R, Morozzi G, Orpianesi C, Cresci A (2004) Effects of different digestible carbohydrates on bile acid metabolism and SCFA production by human gut micro-flora grown in an in vitro semi-continuous culture. Anaerobe 10:19–26
48. Elhardallou SB (1992) The bile acids binding of the fibre-rich fractions of three starchy legumes. Plant Foods Hum Nutr 42:207–218
49. Kim HJ, White PJ (2010) In vitro bile-acid binding and fermentation of high, medium, and low molecular weight beta-glucan. J Agric Food Chem 58:628–634
50. Ridlon JM, Kang DJ, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47:241–259
51. Ayala A, Munoz MF, Arguelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014:360438
52. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11:81–128
53. Hendrickse CW, Kelly RW, Radley S, Donovan IA, Keighley MR, Neoptolemos JP (1994) Lipid peroxidation and prostaglandins in colorectal cancer. Br J Surg 81:1219–1223
54. Leuratti C, Watson MA, Deag EJ, Welch A, Singh R, Gottschalg E, Marnett LJ, Atkin W, Day NE, Shuker DE, Bingham SA (2002) Detection of malondialdehyde DNA adducts in human colorectal mucosa: relationship with diet and the presence of adenomas. Cancer Epidemiol Biomarkers Prev 11:267–273
55. Jenkins DJ, Kendall CW, Marchie A, Josse AR, Nguyen TH, Faulkner DA, Lapsley KG, Blumberg J (2008) Almonds reduce biomarkers of lipid peroxidation in older hyperlipidemic subjects. J Nutr 138:908–913
56. Durak I, Koksal I, Kacmaz M, Buyukkocak S, Cimen BM, Ozturk HS (1999) Hazelnut supplementation enhances plasma antioxidant potential and lowers plasma cholesterol levels. Clin Chim Acta 284:113–115
57. Xie LM, Ge YY, Huang X, Zhang YQ, Li JX (2015) Effects of fermentable dietary fiber supplementation on oxidative and inflammatory status in hemodialysis patients. Int J Clin Exp Med 8:1363–1369
58. Erhardt JG, Lim SS, Bode JC, Bode C (1997) A diet rich in fat and poor in dietary fiber increases the in vitro formation of reactive oxygen species in human feces. J Nutr 127:706–709
59. Wu WT, Chen HL (2011) Konjac glucomannan and inulin systematically modulate antioxidant defense in rats fed a high-fat fiber-free diet. J Agric Food Chem 59:9194–9200
60. Sun J, Hu XL, Le GW, Shi YH (2010) Lactobacilli prevent hydroxy radical production and inhibit Escherichia coli and Enterococcus growth in system mimicking colon fermentation. Lett Appl Microbiol 50:264–269
61. Wang CH, Lai P, Chen ME, Chen HL (2008) Antioxidative capacity produced by Bifidobacterium- and Lactobacillus acidophilus-mediated fermentations of konjac glucomannan and glucomannan oligosaccharides. J Sci Food Agric 88:1294–1300