Skip to main content
Top
Published in: European Journal of Nutrition 8/2018

Open Access 01-12-2018 | Original Contribution

Improvement in cardiometabolic risk markers following a multifunctional diet is associated with gut microbial taxa in healthy overweight and obese subjects

Authors: Nittaya Marungruang, Juscelino Tovar, Inger Björck, Frida Fåk Hållenius

Published in: European Journal of Nutrition | Issue 8/2018

Login to get access

Abstract

Purpose

A multifunctional diet (MFD) targeting subclinical inflammation was developed as a tool to decrease risk factors for cardiometabolic disease in healthy “at-risk” individuals (BMI 25–33 kg/m2). MFD contains several components that are degraded in the colon by the microbiota, such as dietary fibers from rye, barley, oats and berries. It also contains soy beans, oily fish and plant stanols. In previous studies, we have observed improved cardiometabolic markers in healthy at-risk individuals after 4–8 week intake of MFD. However, whether these improvements can be associated with changes in the gut microbiota composition has not been investigated. In the present study, we analyzed the gut microbiota before and after an 8-week dietary intervention with MFD.

Methods

Cardiometabolic at-risk individuals (n = 47), between 51 and 72 years old and with a BMI of 25–33 kg/m2, were given either the MFD or a control diet lacking the functional (“active”) components for 8 weeks in a parallel, randomized design. Next-generation sequencing of bacterial 16S rRNA genes was used to analyze the gut microbiota composition.

Results

The 8-week intervention with MFD did not significantly alter the gut microbiota composition at phylum or genus taxonomic levels, while LEfSE analysis identified increased abundance of Prevotella copri in the MFD group as compared to the control group. Treponema correlated positively with blood pressure. In contrast, Faecalibacterium showed a negative association with blood pressure, while Bilophila appeared to associate with a negative blood lipid profile.

Conclusions

Taken together, results from the present study may be used in the further development of effective dietary concepts capable of reducing cardiometabolic risk markers in humans through a targeted modulation of the gut microbial community.

Trial registration number

Clinical Trials.gov NCT02148653.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bäckhed F, Ding H, Wang T, Hooper L, Koh G, Nagy A, Semenkovich C, Gordon J (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723CrossRefPubMedPubMedCentral Bäckhed F, Ding H, Wang T, Hooper L, Koh G, Nagy A, Semenkovich C, Gordon J (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723CrossRefPubMedPubMedCentral
2.
go back to reference Ley R, Turnbaugh P, Klein S, Gordon J (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023CrossRefPubMed Ley R, Turnbaugh P, Klein S, Gordon J (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023CrossRefPubMed
3.
go back to reference Cani P, Bibiloni R, Knauf C, Waget A, Nevrinck A, Delzenne N, Burcelin R (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57:1470–1481CrossRefPubMed Cani P, Bibiloni R, Knauf C, Waget A, Nevrinck A, Delzenne N, Burcelin R (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57:1470–1481CrossRefPubMed
4.
go back to reference Klinder A, Shen Q, Heppel S, Lovegrove JA, Rowland I, Tuohy KM (2016) Impact of increasing fruit and vegetables and flavonoid intake on the human gut microbiota. Food Funct 7(4):1788–1796. doi:10.1039/c5fo01096a CrossRefPubMed Klinder A, Shen Q, Heppel S, Lovegrove JA, Rowland I, Tuohy KM (2016) Impact of increasing fruit and vegetables and flavonoid intake on the human gut microbiota. Food Funct 7(4):1788–1796. doi:10.​1039/​c5fo01096a CrossRefPubMed
5.
go back to reference Selma MV, Gonzalez-Sarrias A, Salas-Salvado J, Andres-Lacueva C, Alasalvar C, Orem A, Tomas-Barberan FA, Espin JC (2017) The gut microbiota metabolism of pomegranate or walnut ellagitannins yields two urolithin-metabotypes that correlate with cardiometabolic risk biomarkers: Comparison between normoweight, overweight-obesity and metabolic syndrome. Clin Nutr. doi:10.1016/j.clnu.2017.03.012 CrossRefPubMed Selma MV, Gonzalez-Sarrias A, Salas-Salvado J, Andres-Lacueva C, Alasalvar C, Orem A, Tomas-Barberan FA, Espin JC (2017) The gut microbiota metabolism of pomegranate or walnut ellagitannins yields two urolithin-metabotypes that correlate with cardiometabolic risk biomarkers: Comparison between normoweight, overweight-obesity and metabolic syndrome. Clin Nutr. doi:10.​1016/​j.​clnu.​2017.​03.​012 CrossRefPubMed
6.
go back to reference Minihane AM, Vinoy S, Russell WR, Baka A, Roche HM, Tuohy KM, Teeling JL, Blaak EE, Fenech M, Vauzour D, McArdle HJ, Kremer BH, Sterkman L, Vafeiadou K, Benedetti MM, Williams CM, Calder PC (2015) Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr 114(7):999–1012. doi:10.1017/s0007114515002093 CrossRefPubMedPubMedCentral Minihane AM, Vinoy S, Russell WR, Baka A, Roche HM, Tuohy KM, Teeling JL, Blaak EE, Fenech M, Vauzour D, McArdle HJ, Kremer BH, Sterkman L, Vafeiadou K, Benedetti MM, Williams CM, Calder PC (2015) Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr 114(7):999–1012. doi:10.​1017/​s000711451500209​3 CrossRefPubMedPubMedCentral
7.
go back to reference Tovar J, Nilsson A, Johansson M, Ekesbo R, Aberg AM, Johansson U, Bjorck I (2012) A diet based on multiple functional concepts improves cardiometabolic risk parameters in healthy subjects. Nutr Metabol 9:29. doi:10.1186/1743-7075-9-29 CrossRef Tovar J, Nilsson A, Johansson M, Ekesbo R, Aberg AM, Johansson U, Bjorck I (2012) A diet based on multiple functional concepts improves cardiometabolic risk parameters in healthy subjects. Nutr Metabol 9:29. doi:10.​1186/​1743-7075-9-29 CrossRef
8.
go back to reference Tovar J, Johansson M, Bjorck I (2016) A multifunctional diet improves cardiometabolic-related biomarkers independently of weight changes: an 8-week randomized controlled intervention in healthy overweight and obese subjects. Eur J Nutr 55(7):2295–2306. doi:10.1007/s00394-015-1039-2 CrossRefPubMed Tovar J, Johansson M, Bjorck I (2016) A multifunctional diet improves cardiometabolic-related biomarkers independently of weight changes: an 8-week randomized controlled intervention in healthy overweight and obese subjects. Eur J Nutr 55(7):2295–2306. doi:10.​1007/​s00394-015-1039-2 CrossRefPubMed
9.
go back to reference Tovar J, de Mello VD, Nilsson A, Johansson M, Paananen J, Lehtonen M, Hanhineva K, Bjorck I (2017) Reduction in cardiometabolic risk factors by a multifunctional diet is mediated via several branches of metabolism as evidenced by nontargeted metabolite profiling approach. Mol Nutr Food Res. doi:10.1002/mnfr.201600552 CrossRefPubMed Tovar J, de Mello VD, Nilsson A, Johansson M, Paananen J, Lehtonen M, Hanhineva K, Bjorck I (2017) Reduction in cardiometabolic risk factors by a multifunctional diet is mediated via several branches of metabolism as evidenced by nontargeted metabolite profiling approach. Mol Nutr Food Res. doi:10.​1002/​mnfr.​201600552 CrossRefPubMed
10.
go back to reference Nordic Council of Ministers (2014) Nutrition recommendations 2012: integrating nutrition and physical activity. Nordic Council of Ministers, CopenhagenCrossRef Nordic Council of Ministers (2014) Nutrition recommendations 2012: integrating nutrition and physical activity. Nordic Council of Ministers, CopenhagenCrossRef
11.
go back to reference Caporaso J, Kuczynski J, Stombaugh J, Bittinger K, Bushman F, Costello E, Fierer N, Peña A, Goodrich J, Gordon J, Huttley G, Kelley S, Knights D, Koenig J, Ley R, Lozupone C, McDonald D, Muegge B, Pirrung M, Reeder J, Sevinsky J, Turnbaugh P, Walters W, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentral Caporaso J, Kuczynski J, Stombaugh J, Bittinger K, Bushman F, Costello E, Fierer N, Peña A, Goodrich J, Gordon J, Huttley G, Kelley S, Knights D, Koenig J, Ley R, Lozupone C, McDonald D, Muegge B, Pirrung M, Reeder J, Sevinsky J, Turnbaugh P, Walters W, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentral
13.
go back to reference DeSantis T, Hugenholtz P, Larsen N, Rojas M, Brodie E, Keller K, Huber T, Dalevi D, Hu P, Andersen G (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072CrossRefPubMedPubMedCentral DeSantis T, Hugenholtz P, Larsen N, Rojas M, Brodie E, Keller K, Huber T, Dalevi D, Hu P, Andersen G (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072CrossRefPubMedPubMedCentral
15.
go back to reference Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodological) 57(1):289–300 Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodological) 57(1):289–300
16.
go back to reference McDonald JH (2014) Handbook of biological statistics, 3rd edn. Sparky House Publishing, Baltimore, pp 254–260 McDonald JH (2014) Handbook of biological statistics, 3rd edn. Sparky House Publishing, Baltimore, pp 254–260
18.
go back to reference Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821. doi:10.1038/nbt.2676 CrossRefPubMedPubMedCentral Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821. doi:10.​1038/​nbt.​2676 CrossRefPubMedPubMedCentral
20.
go back to reference Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto J-M, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, Torrents D, Ugarte E, Zoetendal EG, Wang J, Guarner F, Pedersen O, de Vos WM, Brunak S, Dore J, Weissenbach J, Ehrlich SD, Bork P (2011) Enterotypes of the human gut microbiome. Nature 473(7346):174–180. doi:10.1038/nature09944 CrossRefPubMedPubMedCentral Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto J-M, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, Torrents D, Ugarte E, Zoetendal EG, Wang J, Guarner F, Pedersen O, de Vos WM, Brunak S, Dore J, Weissenbach J, Ehrlich SD, Bork P (2011) Enterotypes of the human gut microbiome. Nature 473(7346):174–180. doi:10.​1038/​nature09944 CrossRefPubMedPubMedCentral
21.
go back to reference Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with Gut microbial enterotypes. Science 334(6052):105–108. doi:10.1126/science.1208344 CrossRefPubMedPubMedCentral Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with Gut microbial enterotypes. Science 334(6052):105–108. doi:10.​1126/​science.​1208344 CrossRefPubMedPubMedCentral
22.
go back to reference Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee Ying S, De Vadder F, Arora T, Hallen A, Martens E, Björck I, Bäckhed F (2015) Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metabol. doi: 10.1016/j.cmet.2015.10.001 CrossRef Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee Ying S, De Vadder F, Arora T, Hallen A, Martens E, Björck I, Bäckhed F (2015) Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metabol. doi: 10.​1016/​j.​cmet.​2015.​10.​001 CrossRef
23.
go back to reference Matsushita K, Hamaguchi M, Hashimoto M, Yamazaki M, Yamazaki T, Asai K, Yamori M, Bessho K, Toda H, Hasegawa G, Nakamura N, Fukui M (2015) The novel association between red complex of oral microbe and body mass index in healthy Japanese: a population based cross-sectional study. J Clin Biochem Nutr 57(2):135–139. doi:10.3164/jcbn.15-19 CrossRefPubMedPubMedCentral Matsushita K, Hamaguchi M, Hashimoto M, Yamazaki M, Yamazaki T, Asai K, Yamori M, Bessho K, Toda H, Hasegawa G, Nakamura N, Fukui M (2015) The novel association between red complex of oral microbe and body mass index in healthy Japanese: a population based cross-sectional study. J Clin Biochem Nutr 57(2):135–139. doi:10.​3164/​jcbn.​15-19 CrossRefPubMedPubMedCentral
24.
go back to reference Quevrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, Miquel S, Carlier L, Bermudez-Humaran LG, Pigneur B, Lequin O, Kharrat P, Thomas G, Rainteau D, Aubry C, Breyner N, Afonso C, Lavielle S, Grill JP, Chassaing G, Chatel JM, Trugnan G, Xavier R, Langella P, Sokol H, Seksik P (2015) Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut. doi:10.1136/gutjnl-2014-307649 CrossRefPubMed Quevrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, Miquel S, Carlier L, Bermudez-Humaran LG, Pigneur B, Lequin O, Kharrat P, Thomas G, Rainteau D, Aubry C, Breyner N, Afonso C, Lavielle S, Grill JP, Chassaing G, Chatel JM, Trugnan G, Xavier R, Langella P, Sokol H, Seksik P (2015) Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut. doi:10.​1136/​gutjnl-2014-307649 CrossRefPubMed
25.
go back to reference Haro C, Garcia-Carpintero S, Alcala-Diaz JF, Gomez-Delgado F, Delgado-Lista J, Perez-Martinez P, Rangel Zuniga OA, Quintana-Navarro GM, Landa BB, Clemente JC, Lopez-Miranda J, Camargo A, Perez-Jimenez F (2015) The gut microbial community in metabolic syndrome patients is modified by diet. J Nutr Biochem. doi:10.1016/j.jnutbio.2015.08.011 CrossRefPubMed Haro C, Garcia-Carpintero S, Alcala-Diaz JF, Gomez-Delgado F, Delgado-Lista J, Perez-Martinez P, Rangel Zuniga OA, Quintana-Navarro GM, Landa BB, Clemente JC, Lopez-Miranda J, Camargo A, Perez-Jimenez F (2015) The gut microbial community in metabolic syndrome patients is modified by diet. J Nutr Biochem. doi:10.​1016/​j.​jnutbio.​2015.​08.​011 CrossRefPubMed
26.
go back to reference Kumar M, Nagpal R, Kumar R, Hemalatha R, Verma V, Kumar A, Chakraborty C, Singh B, Marotta F, Jain S, Yadav H (2012) Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp Diab Res 2012:902917. doi:10.1155/2012/902917 CrossRef Kumar M, Nagpal R, Kumar R, Hemalatha R, Verma V, Kumar A, Chakraborty C, Singh B, Marotta F, Jain S, Yadav H (2012) Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp Diab Res 2012:902917. doi:10.​1155/​2012/​902917 CrossRef
27.
go back to reference Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 487(7405):104–108. doi:10.1038/nature11225 CrossRefPubMedPubMedCentral Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 487(7405):104–108. doi:10.​1038/​nature11225 CrossRefPubMedPubMedCentral
Metadata
Title
Improvement in cardiometabolic risk markers following a multifunctional diet is associated with gut microbial taxa in healthy overweight and obese subjects
Authors
Nittaya Marungruang
Juscelino Tovar
Inger Björck
Frida Fåk Hållenius
Publication date
01-12-2018
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 8/2018
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-017-1563-3

Other articles of this Issue 8/2018

European Journal of Nutrition 8/2018 Go to the issue