Browse > Article
http://dx.doi.org/10.4014/jmb.1803.03020

Dietary Supplementation with Raspberry Extracts Modifies the Fecal Microbiota in Obese Diabetic db/db Mice  

Garcia-Mazcorro, Jose F. (Research and Development, MNA de Mexico)
Pedreschi, Romina (School of Agronomy, Pontificia Universidad Catolica de Valparaiso)
Chew, Boon (Department of Nutrition and Food Science, Texas A&M University)
Dowd, Scot E. (Molecular Research LP)
Kawas, Jorge R. (Faculty of Agronomy, Universidad Autonoma de Nuevo Leon)
Noratto, Giuliana (Department of Nutrition and Food Science, Texas A&M University)
Publication Information
Journal of Microbiology and Biotechnology / v.28, no.8, 2018 , pp. 1247-1259 More about this Journal
Abstract
Raspberries are polyphenol-rich fruits with the potential to reduce the severity of the clinical signs associated with obesity, a phenomenon that may be related to changes in the gut microbiota. The aim of this study was to investigate the effect of raspberry supplementation on the fecal microbiota using an in vivo model of obesity. Obese diabetic db/db mice were used in this study and assigned to two experimental groups (with and without raspberry supplementation). Fecal samples were collected at the end of the supplementation period (8 weeks) and used for bacterial 16S rRNA gene profiling using a MiSeq instrument (Illumina). QIIME 1.8 was used to analyze the 16S data. Raspberry supplementation was associated with an increased abundance of Lachnospiraceae (p = 0.009), a very important group for gut health, and decreased abundances of Lactobacillus, Odoribacter, and the fiber degrader S24-7 family as well as unknown groups of Bacteroidales and Enterobacteriaceae (p < 0.05). These changes were enough to clearly differentiate bacterial communities accordingly to treatment, based on the analysis of UniFrac distance metrics. However, a predictive approach of functional profiles showed no difference between the treatment groups. Fecal metabolomic analysis provided critical information regarding the raspberry-supplemented group, whose relatively higher phytosterol concentrations may be relevant for the host health, considering the proven health benefits of these phytochemicals. Further studies are needed to investigate whether the observed differences in microbial communities (e.g., Lachnospiraceae) or metabolites relate to clinically significant differences that can prompt the use of raspberry extracts to help patients with obesity.
Keywords
Raspberry; polyphenols; obesity; gut microbiota;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, Keilbaugh SA, et al. 2011. Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108.   DOI
2 Piotr Mazur S, Nes A, Wold AB, Fagertun Remberg S, Aaby K. 2014. Quality and chemical composition of ten red raspberry (Rubus idaeus L.) genotypes during three harvest seasons. Food Chem. 160: 233-240.   DOI
3 Zukiewicz-Sobczak W, Wroblewska P, Zwolinski J, Chmielewska-Badora J, Adamczuk P, Krasowska E, et al. 2014. Obesity and poverty paradox in developed countries. Ann. Agric. Environ. Med. 21: 590-594.   DOI
4 Smith KB, Smith MS. 2016. Obesity statistics. Prim. Care 43: 121-135.   DOI
5 Burton-Freeman BM, Sandhu AK, Edirisinghe I. 2016. Red raspberries and their bioactive polyphenols: cardiometabolic and neuronal health links. Adv. Nutr. 7: 44-65.   DOI
6 McDougall GJ, Stewart D. 2005. The inhibitory effects of berry polyphenols on digestive enzymes. Biofactors 23: 189-195.   DOI
7 Noratto GD, Chew BP, Atienza LM. 2017. Red raspberry (Rubus ideaeus L.) intake decreases oxidative stress in obese diabetic (db/db) mice. Food Chem. 227: 305-314.   DOI
8 Overall J, Bonney SA, Wilson M, Beermann A, Grace MH, Esposito D, et al. 2017. Metabolic effects of berries with structurally diverse anthocyanins. Int. J. Mol. Sci. 18: E422.   DOI
9 Nowak A, Sojka M, Klewicka E, Lipinska L, Klewicki R, Kolodziejczyk K. 2017. Ellagitannins from Rubus idaeus L. exert geno- and cytotoxic effects against human colon adenocarcinoma cell line Caco-2. J. Agric. Food Chem. DOI: 10.1021/acs.jafc.6b05387.   DOI
10 Tun HM, Bridgman SL, Chari R, Field CJ, Guttman DS, Becker AB, et al. 2018. Roles of birth mode and infant gut microbiota in intergenerational transmission of overweight and obesity from mother to offspring. JAMA Pediatr. 172: 368-377.   DOI
11 de la Cuesta-Zuluaga J, Corrales-Agudelo V, Carmona JA, Abad JM, Escobar JS. 2018. Body size phenotypes comprehensively assess cardiometabolic risk and refine the association between obesity and gut microbiota. Int. J. Obes. (Lond.) 42: 424-432.   DOI
12 Worthlet DL, Le Leu RK, Whitehall VL, Conlon M, Christophersen C, Belobrajdic D, et al. 2009. A human, double-blind, placebo-controlled, crossover trial of prebiotic, probiotic, and synbiotic supplementation: effects on luminal, inflammatory, epigenetic, and epithelial biomarkers of colorectal cancer. Am. J. Clin. Nutr. 90: 578-586.   DOI
13 Garcia-Mazcorro JF, Castillo-Carranza SA, Guard B, Gomez-Vazquez JP, Dowd SE, Brightsmith DJ. 2017. Comprehensive molecular characterization of bacterial communities in feces of pet birds using 16S marker sequencing. Microb. Ecol. 73: 224-235.   DOI
14 Saitoh S, Noda S, Aiba Y, Takagi A, Sakamoto M, Benno Y, Koga Y. 2002. Bacteroides ovatus as the predominant commensal intestinal microbe causing a systemic antibody response in inflammatory bowel disease. Clin. Diagn. Lab. Immunol. 9: 54-59.
15 Sekelja M, Berget I, Næs T, Rudi K. 2011. Unveiling an abundant core microbiota in the human adult colon by a phylogroup-independent searching approach. ISME J. 5: 519-531.   DOI
16 Suchodolski JS. 2011. Companion animals symposium: microbes and gastrointestinal health of dogs and cats. J. Anim. Sci. 89: 1520-1530.   DOI
17 Reeves AE, Koenigsknecht MJ, Bergin IL, Young VB. 2012. Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect. Immun. 80: 3786-3794.   DOI
18 Viladomiu M, Hontecillas R, Lu P, Bassaganya-Riera J. 2013. Preventive and prophylactic mechanisms of action of pomegranate bioactive constituents. Evid. Based Complement. Alternat. Med. 2013: 789764.
19 Higashimura Y, Baba Y, Inoue R, Takagi T, Mizushima K, Ohnogi H, et al. 2017. Agaro-oligosaccharides regulate gut microbiota and adipose tissue accumulation in mice. J. Nutr. Sci. Vitaminol. (Tokyo) 63: 269-276.   DOI
20 Fotschki B, Juskiewicz J, Jurgonski A, Rigby N, Sojka M, Kolodziejczyk K, et al. 2017. Raspberry pomace alters cecal microbial activity and reduces secondary bile acids in rats fed a high-fat diet. J. Nutr. Biochem. 46: 13-20.   DOI
21 Ormerod KL, Wood DL, Lachner N, Gellatly SL, Daly JN, Parsons JD, et al. 2016. Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals. Microbiome 4: 36.   DOI
22 Zou X, Yan C, Shi Y, Cao K, Xu J, Wang X, et al. 2014. Mitochondrial dysfunction in obesity-associated nonalcoholic fatty liver disease: the protective effects of pomegranate with its active component punicalagin. Antioxid. Redox Signal. 21: 1557-1570.   DOI
23 Tomas J, Mulet C, Saffarian A, Cavin JB, Ducroc JB, Regnault B, et al. 2016. High-fat diet modifies the PPAR-${\gamma}$ pathway leading to disruption of microbial and physiological ecosystem in murine small intestine. Proc. Natl. Acad. Sci. USA 113: E5934-E5943.   DOI
24 Garcia-Mazcorro J F, Ivanov I, M ills D A, N oratto G . 2016. Influence of whole-wheat consumption on fecal microbial ecology of obese diabetic mice. PeerJ 4: e1702.   DOI
25 Liu X, Zeng B, Zhang J, Li W, Mou F, Wang H, et al. 2016. Role of the gut microbiome in modulating arthritis progression in mice. Sci. Rep. 6: 30594.   DOI
26 Yao J, Carter RA, Vuagniaux G, Barbier M, Rosch JW, Rock CO. 2016. A pathogen-selective antibiotic minimizes disturbance to the microbiome. Antimicrob. Agents Chemother. 60: 4264-4273.   DOI
27 Marangoni F, Poli A. 2010. Phytosterols and cardiovascular health. Pharmacol. Res. 61: 193-199.   DOI
28 Tomas-Barberan FA, Selma MV, Espin JC. 2016. Interactions of gut microbiota with dietary polyphenols and consequences to human health. Curr. Opin. Clin. Nutr. Metab. Care 19: 471-476.   DOI
29 Medjakovic S, Jungbauer A. 2013. Pomegranate: a fruit that ameliorates metabolic syndrome. Food Funct. 4: 19-39.   DOI
30 Heber D, Seeram NP, Wyatt H, Henning SM, Zhang Y, Ogden LG, et al. 2007. Safety and antioxidant activity of a pomegranate ellagitannin-enriched polyphenol dietary supplement in overweight individuals with increased waist size. J. Agric. Food Chem. 55: 10050-10054.   DOI
31 Noratto GD, Garcia-Mazcorro JF, Markel M, Martino HS, Minamoto Y, Steiner JM, et al. 2014. Carbohydrate-free peach (Prunus persica) and plum (Prunus domestica) juice affects fecal microbial ecology in an obese animal model. PLoS One 9: e101723.   DOI
32 Lee HC, Jenner AM, Low CS, Lee YK. 2006. Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota. Res. Microbiol. 157: 876-884.   DOI
33 Bolca S, Van de Wiele T, Possemiers S. 2013. Gut metabotypes govern health effects of dietary polyphenols. Curr. Opin. Biotechnol. 24: 220-225.   DOI
34 Li H, Cao Y. 2010. Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids 39: 1107-1116.   DOI
35 Alam MA, Subhan N, Hossain H, Hossain M, Reza HM, Rahman MM, et al. 2016. Hydroxycinnamic acid derivatives: a potential class of natural compounds for the management of lipid metabolism and obesity. Nutr. Metab. (Lond). 13: 27.   DOI
36 Noratto G, Chew BP, Ivanov I. 2016. Red raspberry decreases heart biomarkers of cardiac remodeling associated with oxidative and inflammatory stress in obese diabetic db/db mice. Food Funct. 7: 4944-4955.   DOI
37 Parkar SG, Stevenson DE, Skinner MA. 2008. The potential influence of fruit polyphenols on colonic microflora and human gut health. Int. J. Food Microbiol. 124: 295-298.   DOI
38 Bialonska D, Ramnani P, Kasimsetty SG, Muntha KR, Gibson GR, Ferreira D. 2010. The influence of pomegranate by-product and punicalagins on selected groups of human intestinal microbiota. Int. J. Food Microbiol. 140: 175-182.   DOI
39 Garcia-Mazcorro JF, Mills DA, Noratto G. 2016. Molecular exploration of fecal microbiome in quinoa-supplemented obese mice. FEMS Microbiol. Ecol. 92: fiw089.   DOI
40 Navas-Molina JA, Peralta-Sanchez JM, Gonzalez A, McMurdie PJ, Vazquez-Baeza Y, Xu Z, et al. 2013. Advancing our understanding of the human microbiome using QIIME. Methods Enzymol. 531: 371-444.
41 DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72: 5069-5072.   DOI
42 Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31: 814-821.   DOI
43 Rideout JR, He Y, Navas-Molina JA, Walters WA, Ursell LK, Gibbons SM, et al. 2014. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ 2: e545.   DOI
44 Wang B, Chandrasekera PC, Pippin JJ. 2014. Leptin- and leptin receptor-deficient rodent models: relevance for human type 2 diabetes. Curr. Diabetes Rev. 10: 131-145.   DOI
45 Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6: 1621-1624.   DOI
46 Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335-336.   DOI
47 Spieker EA, Pyzocha N. 2016. Economic impact of obesity. Prim. Care 43: 83-95.   DOI
48 Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12: R60.   DOI
49 Garcia-Mazcorro JF, Nunes Lage N, Mertens-Talcott S, Talcott S, Chew B, Dowd SE, et al. 2017. Effect of dark sweet cherry powder consumption on the gut microbiota, shortchain fatty acids, and biomarkers of gut health in obese db/db mice. PeerJ 6: e4195.
50 Hammer O, Harper DAT, Ryan PD. 2001. PAST: paleontological statistics software package for education and data analysis. Paleontol. Electron. 4: 1-9.
51 Parks DH, Beiko RG. 2010. Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26: 715-721.   DOI
52 Xia J, Sinelnikov IV, Han B, Wishart DS. 2015. MetaboAnalyst 3.0 - making metabolomics more meaningful. Nucleic Acids Res. 43: W251-W257.   DOI
53 Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11: 265-270.
54 Hill DA, Artis D. 2010. Intestinal bacteria and the regulation of immune cell homeostasis. Annu. Rev. Immunol. 28: 623-667.   DOI
55 Subhan FB, Chan CB. 2016. Review of dietary practices of the 21st century: facts and fallacies. Can. J. Diabetes 40: 348-354.   DOI
56 Clemente JC, Ursell LK, Wegener Parfrey L, Knight R. 2012. The impact of the gut microbiota on human health: an integrative view. Cell 148: 1258-1270.   DOI
57 Dinan TG, Cryan JF. 2016. Microbes, immunity, and behavior: psychoneuroimmunology meets the microbiome. Neuropsychopharmacology 42: 178-192.
58 Harakeh SM, Khan I, Kumosani T, Barbour E, Almasaudi SB, Bahijri SM, et al. 2016. Gut microbiota: a contributing factor to obesity. Front. Cell. Infect. Microbiol. 6: 95.
59 Heiman ML, Greenway FL. 2016. A healthy gastrointestinal microbiome is dependent on dietary diversity. Mol. Metab. 5: 317-320.   DOI