Bread Affects Clinical Parameters and Induces Gut Microbiome-Associated Personal Glycemic Responses

Cell Metabolism

Volumn 25, Issue 6, 2017, Pages 1243-1253.e5

  Korem, Tal ^a   Zeevi, David ^a   Zmora, Niv ^a,b,c   Weissbrod, Omer ^a   Bar, Noam ^a   Lotan Pompan, Maya ^a   Avnit Sagi, Tali ^a   Kosower, Noa ^a   Malka, Gal ^a   Rein, Michal ^a   Suez, Jotham ^a   Goldberg, Ben Z ^a   Weinberger, Adina ^a   Levy, Avraham A ^a   Elinav, Eran ^a   Segal, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

bread; glycemic responses; gut microbiome; nutrition; personalization; prediction

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CREATININE; GAMMA GLUTAMYLTRANSFERASE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LACTATE DEHYDROGENASE; LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ADULT; ARTICLE; BREAD; COMPARATIVE STUDY; CROSSOVER PROCEDURE; DIET; DIETARY INTAKE; FEMALE; FOOD INTAKE; GLYCEMIC CONTROL; HUMAN; INTESTINE FLORA; MALE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RISK FACTOR; WHEAT FLOUR; WHOLE GENOME SEQUENCING; WHOLE GRAIN; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; METABOLISM; MIDDLE AGED; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL;

ADULT; BLOOD GLUCOSE; BREAD; CROSS-OVER STUDIES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; MALE; MIDDLE AGED;

EID: 85020283977     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2017.05.002     Document Type: Article

References (69)

1. Andersson, A., Tengblad, S., Karlström, B., Kamal-Eldin, A., Landberg, R., Basu, S., Aman, P., Vessby, B., Whole-grain foods do not affect insulin sensitivity or markers of lipid peroxidation and inflammation in healthy, moderately overweight subjects. J. Nutr. 137 (2007), 1401–1407.
2. Arendt, E.K., Ryan, L.A.M., Dal Bello, F., Impact of sourdough on the texture of bread. Food Microbiol. 24 (2007), 165–174.
3. Aune, D., Keum, N., Giovannucci, E., Fadnes, L.T., Boffetta, P., Greenwood, D.C., Tonstad, S., Vatten, L.J., Riboli, E., Norat, T., Whole grain consumption and risk of cardiovascular disease, cancer, and all cause and cause specific mortality: systematic review and dose-response meta-analysis of prospective studies. BMJ, 353, 2016, i2716.
4. Bach Kristensen, M., Tetens, I., Alstrup Jørgensen, A.B., Dal Thomsen, A., Milman, N., Hels, O., Sandström, B., Hansen, M., A decrease in iron status in young healthy women after long-term daily consumption of the recommended intake of fibre-rich wheat bread. Eur. J. Nutr. 44 (2005), 334–340.
5. Batt, C.A., Tortorello, M.-L., (eds.) Encyclopedia of Food Microbiology, Second Edition, 2014, Academic Press.
6. Blaak, E.E., Antoine, J.-M., Benton, D., Björck, I., Bozzetto, L., Brouns, F., Diamant, M., Dye, L., Hulshof, T., Holst, J.J., et al. Impact of postprandial glycaemia on health and prevention of disease. Obes. Rev. 13 (2012), 923–984.
7. Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
8. Brownlee, I.A., Moore, C., Chatfield, M., Richardson, D.P., Ashby, P., Kuznesof, S.A., Jebb, S.A., Seal, C.J., Markers of cardiovascular risk are not changed by increased whole-grain intake: the WHOLEheart study, a randomised, controlled dietary intervention. Br. J. Nutr. 104 (2010), 125–134.
9. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 (2010), 335–336.
10. Cavalot, F., Pagliarino, A., Valle, M., Di Martino, L., Bonomo, K., Massucco, P., Anfossi, G., Trovati, M., Postprandial blood glucose predicts cardiovascular events and all-cause mortality in type 2 diabetes in a 14-year follow-up: lessons from the San Luigi Gonzaga Diabetes Study. Diabetes Care 34 (2011), 2237–2243.
11. Chassaing, B., Koren, O., Goodrich, J.K., Poole, A.C., Srinivasan, S., Ley, R.E., Gewirtz, A.T., Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519 (2015), 92–96.
12. Costabile, A., Klinder, A., Fava, F., Napolitano, A., Fogliano, V., Leonard, C., Gibson, G.R., Tuohy, K.M., Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. Br. J. Nutr. 99 (2008), 110–120.
13. David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg, D.B., Button, J.E., Wolfe, B.E., Ling, A.V., Devlin, A.S., Varma, Y., Fischbach, M.A., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505 (2014), 559–563.
14. de Munter, J.S.L., Hu, F.B., Spiegelman, D., Franz, M., van Dam, R.M., Whole grain, bran, and germ intake and risk of type 2 diabetes: a prospective cohort study and systematic review. PLoS Med., 4, 2007, e261.
15. Edgar, R.C., UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10 (2013), 996–998.
16. FAO (Food and Agriculture Organization of the United Nations) (1998). FAOSTAT Statistical Database. http://www.fao.org/faostat/en/#home.
17. Foster-Powell, K., Holt, S.H.A., Brand-Miller, J.C., International table of glycemic index and glycemic load values: 2002. Am. J. Clin. Nutr. 76 (2002), 5–56.
18. Friedman, J.H., Greedy function approximation: a gradient boosting machine. Ann. Stat. 29 (2001), 1189–1232.
19. Gallwitz, B., Implications of postprandial glucose and weight control in people with type 2 diabetes: understanding and implementing the International Diabetes Federation guidelines. Diabetes Care 32:Suppl 2 (2009), S322–S325.
20. Garcia-Mazcorro, J.F., Ivanov, I., Mills, D.A., Noratto, G., Influence of whole-wheat consumption on fecal microbial community structure of obese diabetic mice. PeerJ, 4, 2016, e1702.
21. Giacco, R., Clemente, G., Cipriano, D., Luongo, D., Viscovo, D., Patti, L., Di Marino, L., Giacco, A., Naviglio, D., Bianchi, M.A., et al. Effects of the regular consumption of wholemeal wheat foods on cardiovascular risk factors in healthy people. Nutr. Metab. Cardiovasc. Dis. 20 (2010), 186–194.
22. Jacobs, D.R. Jr., Marquart, L., Slavin, J., Kushi, L.H., Whole-grain intake and cancer: an expanded review and meta-analysis. Nutr. Cancer 30 (1998), 85–96.
23. Jenkins, D.J., Wolever, T.M., Taylor, R.H., Barker, H., Fielden, H., Baldwin, J.M., Bowling, A.C., Newman, H.C., Jenkins, A.L., Goff, D.V., Glycemic index of foods: a physiological basis for carbohydrate exchange. Am. J. Clin. Nutr. 34 (1981), 362–366.
24. Jensen, M.K., Koh-Banerjee, P., Franz, M., Sampson, L., Grønbaek, M., Rimm, E.B., Whole grains, bran, and germ in relation to homocysteine and markers of glycemic control, lipids, and inflammation 1. Am. J. Clin. Nutr. 83 (2006), 275–283.
25. th edition, by George W. Snedecor and William G. Cochran. J. Educ. Behav. Stat. 19 (1994), 304–307.
26. Kanehisa, M., Goto, S., KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28 (2000), 27–30.
27. Karlsson, F.H., Tremaroli, V., Nookaew, I., Bergström, G., Behre, C.J., Fagerberg, B., Nielsen, J., Bäckhed, F., Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498 (2013), 99–103.
28. Katcher, H.I., Legro, R.S., Kunselman, A.R., Gillies, P.J., Demers, L.M., Bagshaw, D.M., Kris-Etherton, P.M., The effects of a whole grain-enriched hypocaloric diet on cardiovascular disease risk factors in men and women with metabolic syndrome. Am. J. Clin. Nutr. 87 (2008), 79–90.
29. Kenward, M.G., Jones, B., The 2x2 cross-over trial. Design and Analysis of Cross-Over Trials, Second Edition, 2003, Chapman and Hall/CRC.
30. Korem, T., Zeevi, D., Suez, J., Weinberger, A., Avnit-Sagi, T., Pompan-Lotan, M., Matot, E., Jona, G., Harmelin, A., Cohen, N., et al. Growth dynamics of gut microbiota in health and disease inferred from single metagenomic samples. Science 349 (2015), 1101–1106.
31. Kovatcheva-Datchary, P., Nilsson, A., Akrami, R., Lee, Y.S., De Vadder, F., Arora, T., Hallen, A., Martens, E., Björck, I., Bäckhed, F., Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab. 22 (2015), 971–982.
32. Lamkin, D.M., Spitz, D.R., Shahzad, M.M.K., Zimmerman, B., Lenihan, D.J., Degeest, K., Lubaroff, D.M., Shinn, E.H., Sood, A.K., Lutgendorf, S.K., Glucose as a prognostic factor in ovarian carcinoma. Cancer 115 (2009), 1021–1027.
33. Lappi, J., Selinheimo, E., Schwab, U., Katina, K., Lehtinen, P., Mykkänen, H., Kolehmainen, M., Poutanen, K., Sourdough fermentation of wholemeal wheat bread increases solubility of arabinoxylan and protein and decreases postprandial glucose and insulin responses. J. Cereal Sci. 51 (2010), 152–158.
34. Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.-M., Kennedy, S., et al., MetaHIT consortium. Richness of human gut microbiome correlates with metabolic markers. Nature 500 (2013), 541–546.
35. Leenhardt, F., Levrat-Verny, M.-A., Chanliaud, E., Rémésy, C., Moderate decrease of pH by sourdough fermentation is sufficient to reduce phytate content of whole wheat flour through endogenous phytase activity. J. Agric. Food Chem. 53 (2005), 98–102.
36. Li, J., Jia, H., Cai, X., Zhong, H., Feng, Q., Sunagawa, S., Arumugam, M., Kultima, J.R., Prifti, E., Nielsen, T., et al. MetaHIT Consortium, MetaHIT Consortium. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 32 (2014), 834–841.
37. Lin, H.V., Frassetto, A., Kowalik, E.J. Jr., Nawrocki, A.R., Lu, M.M., Kosinski, J.R., Hubert, J.A., Szeto, D., Yao, X., Forrest, G., Marsh, D.J., Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS ONE, 7, 2012, e35240.
38. Lopez, H.W., Duclos, V., Coudray, C., Krespine, V., Feillet-Coudray, C., Messager, A., Demigné, C., Rémésy, C., Making bread with sourdough improves mineral bioavailability from reconstituted whole wheat flour in rats. Nutrition 19 (2003), 524–530.
39. Lupton, J.R., Microbial degradation products influence colon cancer risk: the butyrate controversy. J. Nutr. 134 (2004), 479–482.
40. Lutsey, P.L., Jacobs, D.R. Jr., Kori, S., Mayer-Davis, E., Shea, S., Steffen, L.M., Szklo, M., Tracy, R., Whole grain intake and its cross-sectional association with obesity, insulin resistance, inflammation, diabetes and subclinical CVD: the MESA study. Br. J. Nutr. 98 (2007), 397–405.
41. Mandal, S., Van Treuren, W., White, R.A., Eggesbø, M., Knight, R., Peddada, S.D., Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb. Ecol. Health Dis., 26, 2015, 10.3402/mehd.v26.27663.
42. Marco-Sola, S., Sammeth, M., Guigó, R., Ribeca, P., The GEM mapper: fast, accurate and versatile alignment by filtration. Nat. Methods 9 (2012), 1185–1188.
43. Matthan, N.R., Ausman, L.M., Meng, H., Tighiouart, H., Lichtenstein, A.H., Estimating the reliability of glycemic index values and potential sources of methodological and biological variability. Am. J. Clin. Nutr. 104 (2016), 1004–1013.
44. McCance, R.A., Widdowson, E.M., Mineral metabolism of healthy adults on white and brown bread dietaries. J. Physiol. 101 (1942), 44–85.
45. Mehrotra, D.V., A recommended analysis for 2 × 2 crossover trials with baseline measurements. Pharm. Stat. 13 (2014), 376–387.
46. Mellen, P.B., Walsh, T.F., Herrington, D.M., Whole grain intake and cardiovascular disease: a meta-analysis. Nutr. Metab. Cardiovasc. Dis. 18 (2008), 283–290.
47. Mente, A., de Koning, L., Shannon, H.S., Anand, S.S., A systematic review of the evidence supporting a causal link between dietary factors and coronary heart disease. Arch. Intern. Med. 169 (2009), 659–669.
48. Minervini, F., De Angelis, M., Di Cagno, R., Gobbetti, M., Ecological parameters influencing microbial diversity and stability of traditional sourdough. Int. J. Food Microbiol. 171 (2014), 136–146.
49. Montonen, J., Boeing, H., Fritsche, A., Schleicher, E., Joost, H.-G., Schulze, M.B., Steffen, A., Pischon, T., Consumption of red meat and whole-grain bread in relation to biomarkers of obesity, inflammation, glucose metabolism and oxidative stress. Eur. J. Nutr. 52 (2013), 337–345.
50. Muñoz-Tamayo, R., Laroche, B., Walter, E., Doré, J., Duncan, S.H., Flint, H.J., Leclerc, M., Kinetic modelling of lactate utilization and butyrate production by key human colonic bacterial species. FEMS Microbiol. Ecol. 76 (2011), 615–624.
51. Nishida, T., Tsuji, S., Tsujii, M., Arimitsu, S., Haruna, Y., Imano, E., Suzuki, M., Kanda, T., Kawano, S., Hiramatsu, N., et al. Oral glucose tolerance test predicts prognosis of patients with liver cirrhosis. Am. J. Gastroenterol. 101 (2006), 70–75.
52. Pereira, M.A., Jacobs, D.R. Jr., Pins, J.J., Raatz, S.K., Gross, M.D., Slavin, J.L., Seaquist, E.R., Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults. Am. J. Clin. Nutr. 75 (2002), 848–855.
53. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
54. Reinhold, J.G., Faradji, B., Abadi, P., Ismail-Beigi, F., Decreased absorption of calcium, magnesium, zinc and phosphorus by humans due to increased fiber and phosphorus consumption as wheat bread. J. Nutr. 106 (1976), 493–503.
55. Salamini, F., Ozkan, H., Brandolini, A., Schäfer-Pregl, R., Martin, W., Genetics and geography of wild cereal domestication in the near east. Nat. Rev. Genet. 3 (2002), 429–441.
56. Segain, J.P., Raingeard de la Blétière, D., Bourreille, A., Leray, V., Gervois, N., Rosales, C., Ferrier, L., Bonnet, C., Blottière, H.M., Galmiche, J.P., Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 47 (2000), 397–403.
57. Slavin, J.L., Jacobs, D., Marquart, L., Wiemer, K., The role of whole grains in disease prevention. J. Am. Diet. Assoc. 101 (2001), 780–785.
58. Sofi, F., Ghiselli, L., Cesari, F., Gori, A.M., Mannini, L., Casini, A., Vazzana, C., Vecchio, V., Gensini, G.F., Abbate, R., Benedettelli, S., Effects of short-term consumption of bread obtained by an old Italian grain variety on lipid, inflammatory, and hemorheological variables: an intervention study. J. Med. Food 13 (2010), 615–620.
59. Suez, J., Korem, T., Zeevi, D., Zilberman-Schapira, G., Thaiss, C.A., Maza, O., Israeli, D., Zmora, N., Gilad, S., Weinberger, A., et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514 (2014), 181–186.
60. Tighe, P., Duthie, G., Vaughan, N., Brittenden, J., Simpson, W.G., Duthie, S., Mutch, W., Wahle, K., Horgan, G., Thies, F., Effect of increased consumption of whole-grain foods on blood pressure and other cardiovascular risk markers in healthy middle-aged persons: a randomized controlled trial. Am. J. Clin. Nutr. 92 (2010), 733–740.
61. Tims, S., Derom, C., Jonkers, D.M., Vlietinck, R., Saris, W.H., Kleerebezem, M., de Vos, W.M., Zoetendal, E.G., Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J. 7 (2013), 707–717.
62. Truong, D.T., Franzosa, E.A., Tickle, T.L., Scholz, M., Weingart, G., Pasolli, E., Tett, A., Huttenhower, C., Segata, N., MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat. Methods 12 (2015), 902–903.
63. Tucker, A.J., Mackay, K.A., Robinson, L.E., Graham, T.E., Bakovic, M., Duncan, A.M., The effect of whole grain wheat sourdough bread consumption on serum lipids in healthy normoglycemic/normoinsulinemic and hyperglycemic/hyperinsulinemic adults depends on presence of the APOE E3/E3 genotype: a randomized controlled trial. Nutr. Metab. (Lond.), 7, 2010, 37.
64. Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R., Gordon, J.I., An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 (2006), 1027–1031.
65. USDA (United States Department of Agriculture) (2016). World Agricultural Supply and Demand Estimates. https://www.usda.gov/oce/commodity/wasde/.
66. Vanegas, S.M., Meydani, M., Barnett, J.B., Goldin, B., Kane, A., Rasmussen, H., Brown, C., Vangay, P., Knights, D., Jonnalagadda, S., et al. Substituting whole grains for refined grains in a 6-wk randomized trial has a modest effect on gut microbiota and immune and inflammatory markers of healthy adults. Am. J. Clin. Nutr. 105 (2017), 635–650.
67. Vitaglione, P., Mennella, I., Ferracane, R., Rivellese, A.A., Giacco, R., Ercolini, D., Gibbons, S.M., La Storia, A., Gilbert, J.A., Jonnalagadda, S., et al. Whole-grain wheat consumption reduces inflammation in a randomized controlled trial on overweight and obese subjects with unhealthy dietary and lifestyle behaviors: role of polyphenols bound to cereal dietary fiber. Am. J. Clin. Nutr. 101 (2015), 251–261.
68. Zeevi, D., Korem, T., Zmora, N., Israeli, D., Rothschild, D., Weinberger, A., Ben-Yacov, O., Lador, D., Avnit-Sagi, T., Lotan-Pompan, M., et al. Personalized nutrition by prediction of glycemic responses. Cell 163 (2015), 1079–1094.
69. Zhang, X., Shen, D., Fang, Z., Jie, Z., Qiu, X., Zhang, C., Chen, Y., Ji, L., Human gut microbiota changes reveal the progression of glucose intolerance. PLoS ONE, 8, 2013, e71108.