Whole rye consumption improves blood and liver n-3 fatty acid profile and gut microbiota composition in rats

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Ounnas, Fayçal ^a,b,c   Privé, Florence ^a,b,c   Salen, Patricia ^a   Gaci, Nadia ^d   Tottey, William ^d   Calani, Luca ^e   Bresciani, Letizia ^e   López Gutiérrez, Noelia ^g   Hazane Puch, Florence ^f   Laporte, François ^f   Brugère, Jean François ^d   Del Rio, Daniele ^e   Demeilliers, Christine ^b,c   De Lorgeril, Michel ^a  

^a LABORATOIRE TIMC IMAG   (France)

^b UNIV GRENOBLE ALPES   (France)

^c INSERM   (France)

^d UNIVERSITÉ CLERMONT AUVERGNE   (France)

^e UNIVERSITY OF PARMA   (Italy)

^f GRENOBLE UNIVERSITY HOSPITAL   (France)

^g UNIVERSITY OF ALMERÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; BUTYRIC ACID; DOCOSAHEXAENOIC ACID; ENTEROLACTONE; ICOSAPENTAENOIC ACID; LONG CHAIN FATTY ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; POLYPHENOL; SHORT CHAIN FATTY ACID;

ANIMAL EXPERIMENT; ARTICLE; BACTEROIDETES; BODY WEIGHT; CECUM; CLOSTRIDIALES; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FAT INTAKE; FATTY ACID ANALYSIS; FATTY ACID METABOLISM; FECES ANALYSIS; FIRMICUTES; FOOD COMPOSITION; FOOD INTAKE; INTESTINE FLORA; LIPID BLOOD LEVEL; LIPID LIVER LEVEL; MACRONUTRIENT; MALE; NONHUMAN; RAT; REFINED RYE; RYE; URINARY EXCRETION; WHOLE RYE; ANIMAL; BLOOD; CHEMISTRY; DIET; DNA MICROARRAY; FECES; FEEDING BEHAVIOR; INTESTINE; LIVER; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; SECALE; WISTAR RAT;

ANIMALS; BODY WEIGHT; CECUM; DIET; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; FECES; FEEDING BEHAVIOR; GASTROINTESTINAL MICROBIOME; INTESTINES; LIVER; MALE; MASS SPECTROMETRY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYPHENOLS; RATS; RATS, WISTAR; SECALE;

EID: 84959431422     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148118     Document Type: Article

References (61)

1. Wu H, Flint AJ, Qi Q, van Dam RM, Sampson LA, Rimm EB, et al. Association between dietary whole grain intake and risk of mortality. JAMA Intern Med. 2015; 175(3):373-384. doi: 10.1001/jamainternmed.2014.6283 PMID: 25559238
2. Bartłomiej S, Justyna RK, Ewa N. Bioactive compounds in cereal grains-occurrence, structure, technological significance and nutritional benefits-A review. Food Sci Technol Int. 2012; 18: 559-568. doi: 10.1177/1082013211433079 PMID: 23064524
3. Belobrajdic DP, Bird AR The potential role of phytochemicals in wholegrain cereals for the prevention of type-2 diabetes. Nutr J. 2013; 12:62. doi: 10.1186/1475-2891-12-62 PMID: 23679924
4. Frølich W, Aman P, Tetens I. Whole grain foods and health-A Scandinavian perspective. Food Nutr Res. 2013; 57: 18503.
5. Kyrø C, Skeie G, Dragsted LO, Christensen J, Overvad K, Hallmans G, et al. Intake of whole grain in Scandinavia: intake, sources and compliance with new national recommendations. Scand J Public Health. 2012; 40(1):76-84. doi: 10.1177/1403494811421057 PMID: 21976053
6. Glitsø LV, Mazur WM, Adlercreutz H, Wähälä K, Mäkelä T, Sandström B, et al. Intestinal metabolism of rye lignans in pigs. Br J Nutr. 2000; 84(4):429-37. PMID: 11103213
7. Nilsson M, Åman P, Härkönen H, Hallmans G, Knudsen KEB, Mazur W, et al. Content of nutrients and lignans in roller milled fractions of rye. J Sc of Food and Agri. 1997; 73(2): 143-148.
8. Juntunen KS, Mazur WM, Liukkonen KH, Uehara M, Poutanen KS, Adlercreutz HC, et al. Consumption of whole meal rye bread increases serum concentrations and urinary excretion of enterolactone compared with consumption of white wheat bread in healthy Finnish men and women. Br J Nutr. 2000; 84 (6):839-46. PMID: 11177200
9. Superko HR, Superko SM, Nasir K, Agatson A, Garrett BC. Omega-3 fatty acid blood levels. Clinical significance and controversy. Circulation. 2013; 128:2154-61. doi: 10.1161/CIRCULATIONAHA.113. 002731 PMID: 24190935
10. Childs CE, Romeu-Nadal M, Burdge GC, Calder PC. Gender differences in the n-3 fatty acid content of tissues. Proc Nutr Soc. 2008; 67(1):19-27. doi: 10.1017/S0029665108005983 PMID: 18234128
11. Burdge GC, Calder PC. Conversion of alpha-linolenic acid to longer-chain polyunsaturated fatty acids in human adults. Review. Reprod Nutr Dev. 2005; 45(5):581-97. PMID: 16188209
12. Sibbons CM, Brenna JT, Lawrence P, Hoile SP, Clarke-Harris R, Lillycrop KA, et al. Effect of sex hormones on n-3 polyunsaturated fatty acid biosynthesis in HepG2 cells and in human primary hepatocytes. Prostaglandins Leukot Essent Fatty Acids. 2014; 90(2-3):47-54. doi: 10.1016/j.plefa.2013.12. 006 PMID: 24411721
13. Toufektsian MC, Salen P, Tonelli C, de Lorgeril M. Dietary flavonoids increase plasma very long-chain (n-3) fatty acids in rats. J Nutr. 2011; 141:37-41. doi: 10.3945/jn.110.127225 PMID: 21068183
14. Ounnas F, Privé F, Salen P, Hazane-Puch F, Laporte F, Fontaine E, et al. Wheat aleurone polyphenols increase plasma eicosapentaenoic acid in rats. Food Nutr Res. 2014; 58: 24604.
15. Le Gall M, Serena A, Jørgensen H, Theil PK, Bach Knudsen KE. The role of whole-wheat grain and wheat and rye ingredients on the digestion and fermentation processes in the gut-A model experiment with pigs. Br J Nutr. 2009; 102(11):1590-600. doi: 10.1017/S0007114509990924 PMID: 19635175
16. Theil PK, Jørgensen H, Serena A, Hendrickson J, Bach Knudsen KE. Products deriving from microbial fermentation are linked to insulinaemic response in pigs fed breads prepared from whole-wheat grain and wheat and rye ingredients. Br J Nutr. 2011; 105(3):373-83. doi: 10.1017/S0007114510003715 PMID: 20923581
17. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012; 489(7415):220-30. doi: 10.1038/nature11550 PMID: 22972295
18. Glitsø LV, Brunsgaard G, Højsgaard S, Sandström B, Bach Knudsen KE. Intestinal degradation in pigs of rye dietary fibre with different structural characteristics. Br J Nutr. 1998; 80(5):457-68. PMID: 9924268
19. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. 2006; 40(3):235-43. PMID: 16633129
20. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ, et al. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008; 15; 27(2):104-19. PMID: 17973645
21. Everard A, Cani PD. Diabetes, obesity and gut microbiota. Best Pract Res Clin Gastroenterol. 2013; 27 (1):73-83. doi: 10.1016/j.bpg.2013.03.007 PMID: 23768554
22. Zhao L. The gut microbiota and obesity: from correlation to causality. Nat Rev Microbiol. 2013; 11 (9):639-47. doi: 10.1038/nrmicro3089 PMID: 23912213
23. Freeland KR, Wilson C, Wolever TM. Adaptation of colonic fermentation and glucagon-like peptide-1 secretion with increased wheat fibre intake for 1 year in hyperinsulinaemic human subjects. Br J Nutr. 2010; 103(1):82-90. doi: 10.1017/S0007114509991462 PMID: 19664300
24. Hallmans G, Zhang JX, Lundin E, Stattin P, Johansson A, Johansson I, et al. Rye, lignans and human health. Proc Nutr. 2003; Soc 62: 193-119.
25. Reeves PG, Nielsen FH, Fahey GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of 365 Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123: 193951.
26. di Giuseppe R, de Lorgeril M, Salen P, Laporte F, Di Castelnuovo A, Krogh V, et al. Alcohol consumption and n-3 polyunsaturated fatty acids in healthy men and women from 3 European populations. Am J Clin Nutr. 2009; 89:354-62. doi: 10.3945/ajcn.2008.26661 PMID: 19056552
27. de Lorgeril M, Salen P, Martin JL, Boucher F, de Leiris J. Interactions of wine drinking with omega-3 fatty acids in patients with coronary heart disease: a fish-like effect of moderate wine drinking. Am Heart J. 2008; 155:175-81. PMID: 18082510
28. Calani L, Ounnas F, Salen P, Demeilliers C, Bresciani L, Brighenti F, et al. Bioavailability and metabolism of hydroxycinnamates in rats fed with durum wheat aleurone fractions. Food Funct. 2014; 23; 5 (8):1738-46. doi: 10.1039/c4fo00328d PMID: 24977665
29. Tottey W, Denonfoux J, Jaziri F, Parisot N, Missaoui M, Hill DRC, et al. The human gut chip "HuGChip", an explorative phylogenetic microarray for determining gut microbiome diversity at family level. PLoS One. 2013; 17; 8(5):e62544. doi: 10.1371/journal.pone.0062544 PMID: 23690942
30. Feria-Gervasio D, Denis S, Alric M, Brugère JF. In vitro maintenance of a human proximal colon microbiota using the continuous fermentation system P-ECSIM. Appl Microbiol Biotechnol. 2011; 91 (5):1425-33. doi: 10.1007/s00253-011-3462-5 PMID: 21773764
31. Hammer Ø, Haprper DAT, Ryan PD. Paleontological statistics software package for education and data analysis. Palaeontologia Electronica. 2001; 4(1): 4-8.
32. Andreasen MF, Kroon PA, Williamson G, Garcia-Conesa MT. Esterase activity able to hydrolyze dietary antioxidant hydroxycinnamates is distributed along the intestine of mammals. J Agric Food Chem. 2001; 49(11):5679-84. PMID: 11714377
33. Andreasen MF, Christensen LP, Meyer AS, Hansen A. Content of phenolic acids and ferulic acid dehydrodimers in 17 rye (Secale cereale L.) varieties. J Agric Food Chem. 2000; 48(7):2837-42. PMID: 11032481
34. Nordlund E, Aura AM, Mattila I, Kössö T, Rouau X, Poutanen K, et al. Formation of phenolic microbial metabolites and short-chain fatty acids from rye, wheat, and oat bran and their fractions in the metabolical in vitro colon model. J Agric Food Chem. 2012; 22; 60(33):8134-45. doi: 10.1021/jf3008037 PMID: 22731123
35. Parkar SG, Trower TM, Stevenson DE. Fecal microbial metabolism of polyphenols and its effects on human gut microbiota. Anaerobe. 2013; 23:12-9. doi: 10.1016/j.anaerobe.2013.07.009 PMID: 23916722
36. Landete JM. Plant and mammalian lignans: a review of source, intake, metabolism, intestinal bacteria and health. Food Res Int. 2012; 46:410-424
37. Lankinen M, Schwab U, Gopalacharyulu PV, Seppänen-Laakso T, Yetukuri L, Sysi-Aho M, et al. Dietary carbohydrate modification alters serum metabolic profiles in individuals with the metabolic syndrome. Nutr Metab Cardiovasc Dis. 2010; 20(4):249-57. doi: 10.1016/j.numecd.2009.04.009 PMID: 19553094
38. Emken EA. Stable isotope approaches, applications and issues related to polyunsaturated fatty acid metabolism studies. Lipids. 2001; 36: 965-973. PMID: 11724469
39. Giltay EJ, Gooren LJ, Toorians AW, Katan MB, Zock PL. Docosahexaenoic acid concentrations are higher in women than in men because of estrogenic effects. Am J Clin Nutr. 2004; 80:1167-74. PMID: 15531662
40. Burdge GC, Wootton SAConversion of alpha-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. Br J Nutr. 2002; 88(4):411-20. PMID: 12323090
41. Burdge GC, Jones AE, Wootton SA Eicosapentaenoic and docosapentaenoic acids are the principal products of alpha-linolenic acid metabolism in young men. Br J Nutr. 2002; 88(4):355-63. PMID: 12323085
42. Pawlosky R, Hibbeln J, Lin Y, Salem N. n-3 fatty acid metabolism in women. Br J Nutr. 2003; 90 (5):993-4; 994-5. PMID: 14667193
43. Penttinen P, Jaehrling J, Damdimopoulos AE, Inzunza J, Lemmen JG, van der Saag P, et al. Diet derived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator. Endocrinology. 2007; 148:4875-86. PMID: 17628008
44. Damdimopoulou P, Nurmi T, Salminen A, Damdimopoulos AE, Kotka M, van der Saag P, et al. A single dose of enterolactone activates estrogen signaling and regulates expression of circadian clock genes in mice. J Nutr. 2011; 141(9):1583-9. doi: 10.3945/jn.111.140277 PMID: 21753063
45. Gobert M, Martin B, Ferlay A, Chilliard Y, Graulet B, Pradel P, et al. Plant polyphenols associated with vitamin E can reduce plasma lipoperoxidation in dairy cows given n-3 polyunsaturated fatty acids. J Dairy Sci. 2009; 92(12):6095-104. doi: 10.3168/jds.2009-2087 PMID: 19923612
46. Martínez-Ramírez HR, Kramer JK, de Lange CF. Ileal flows and apparent ileal digestibility of fatty acids in growing gilts fed flaxseed containing diets. J Anim Sci. 2013; 91(6):2729-39. doi: 10.2527/jas.2012-5783 PMID: 23478834
47. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013; 500:541-546. doi: 10.1038/nature12506 PMID: 23985870
48. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012; 488:178-184. doi: 10.1038/nature11319 PMID: 22797518
49. Bervoets L, Van Hoorenbeeck K, Kortleven I, Van Noten C, Hens N, Vael C, et al. Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathog. 2013; 5(1):10. doi: 10.1186/1757-4749-5-10 PMID: 23631345
50. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444(7122):1027-31. PMID: 17183312
51. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008; 3:213-23. doi: 10.1016/j. chom.2008.02.015 PMID: 18407065
52. Caricilli AM, Saad MJ. The role of gut microbiota on insulin resistance. Nutrients. 2013; 5(3):829-51. doi: 10.3390/nu5030829 PMID: 23482058
53. Matijašić BB, Obermajer T, Lipoglavšek L, Grabnar I, Avguštin G, Rogelj I. Association of dietary type with fecal microbiota in vegetarians and omnivores in Slovenia. Eur J Nutr. 2014; 53(4):1051-64. doi: 10.1007/s00394-013-0607-6 PMID: 24173964
54. Unno T, Sakuma M, Mitsuhashi S. Effect of dietary supplementation of (-)-epigallocatechin gallate on gut microbiota and biomarkers of colonic fermentation in rats. J Nutr Sci Vitaminol (Tokyo). 2014; 60 (3):213-9.
55. Boto-Ordóñez M, Urpi-Sarda M, Queipo-Ortuño MI, Tulipani S, Tinahones FJ, Andres-Lacueva C. High levels of Bifidobacteria are associated with increased levels of anthocyanin microbial metabolites: a randomized clinical trial. Food Funct. 2014; 5:1932-1938. doi: 10.1039/c4fo00029c PMID: 24958563
56. Czank C, Cassidy A, Zhang Q, Morrison DJ, Preston T, Kroon PA, et al. Human metabolism and elimination of the anthocyanin, cyanidin-3-glucoside: a (13)C-tracer study. Am J Clin Nutr. 2013; 97:995-1003. doi: 10.3945/ajcn.112.049247 PMID: 23604435
57. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010; 107(33):14691-6. doi: 10.1073/pnas.1005963107 PMID: 20679230
58. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012; 486(7402):222-7. doi: 10.1038/nature11053 PMID: 22699611
59. Lappi J, Salojärvi J, Kolehmainen M, Mykkänen H, Poutanen K, de Vos WM, et al. Intake of whole-grain and fiber-rich rye bread versus refined wheat bread does not differentiate intestinal microbiota composition in Finnish adults with metabolic syndrome. J Nutr. 2013; 143(5):648-55. doi: 10.3945/jn.112. 172668 PMID: 23514765
60. Carbonero F, Benefiel AC, Alizadeh-Ghamsari AH, Gaskins HR. Microbial pathways in colonic sulfur metabolism and links with health and disease. Front Physiol. 2012; 3:448. doi: 10.3389/fphys.2012. 00448 PMID: 23226130
61. Rey FE, Gonzalez MD, Cheng J, Wu M, Ahern PP, Gordon JI, et al. Metabolic niche of a prominent sulfate-reducing human gut bacterium. Proc Natl Acad Sci U S A. 2013; 110(33):13582-7. doi: 10.1073/pnas.1312524110 PMID: 23898195