Dietary fibers of Canna edulis and Maranta arundinacea rhizomes ameliorate metabolic diseases and gut dysbiosis in mice fed a high-fat diet

Putra Santoso, Rita Maliza

Abstract


Background and purpose: Canna edulis (C. edulis) and Maranta arundinacea (M. arundinacea) are potential medicinal plants. This study investigated the preventive effect of dietary fibers from C. edulis and                                 M. arundinacea rhizomes against metabolic diseases and gut dysbiosis promoted by a high-fat diet (HFD).

Experimental approach: Twenty-four male mice were divided into 4 groups and fed a low-fat diet, HFD, or HFD combined with 10% C. edulis fiber or M. arundinacea fiber for 12 weeks. Subsequently, the indicators of metabolic syndromes and gut microbiota composition were investigated.

Findings/Results: C. edulis fiber effectively prevented obesity and counteracted HFD-induced dyslipidemia. C. edulis and M. arundinacea fibers prevented type 2 diabetes, but C. edulis fiber was more effective in regulating glucose tolerance and insulin than M. arundinacea. C. edulis fiber also reduced steatosis and inflammation in the liver. 16S rRNA sequencing of fecal microbiota revealed that the fibers decreased the abundance of Desulfobacterota, but only C. edulis increased Bacteroidota while decreasing Firmicutes.                      C. edulis fiber elevated the abundance of beneficial microbiota, including Lactobacilus reuteri, L. johnsonii, and Bacteroides fragilis, while lowering the pathogenic species Mucispirillum sp. Otherwise, M. arundinacea fiber increased the beneficial species L. murinus and Faecalibacterium prausnitzii, and pathogenic species Mucispirillum sp.

Conclusion and implications: C. edulis and M. arundinacea fibers exerted ameliorative effects against metabolic diseases and gut dysbiosis caused by HFD. However, C. edulis fiber was more effective than                        M. arundinacea. Therefore, C. edulis fiber could be a candidate for supplements preventing metabolic diseases and gut dysbiosis.

 

 


Keywords


Desulfobacterota; Dyslipidemia; Hepatic steatosis; Hyperinsulinemia; Metabolic syndromes; Mucispirillum.

Full Text:

PDF

References


Zhang J, Wang ZW. Soluble dietary fiber from Canna edulis Ker by-product and its physicochemical properties. Carbohydr Polym. 2013; 92(1):289-296.DOI: 10.1016/j.carbpol.2012.09.067.

Xie F, Gong S, Zhang W, Wu J, Wang Z. Potential of lignin from Canna edulis ker residue in the inhibition of α-d-glucosidase: kinetics and interaction mechanism merging with docking simulation. Int J Biol Macromol. 2017;95:592-602.DOI: 10.1016/j.ijbiomac.2016.11.100.

Tarique J, Sapuan SM, Khalina A, Ilyas RA, Zainudin ES. Thermal, flammability, and antimicrobial properties of arrowroot (Maranta arundinacea) fiber reinforced arrowroot starch biopolymer composites for food packaging applications. Int J Biol Macromol. 2022;213:1-10.DOI: 10.1016/j.ijbiomac.2022.05.104.

Malesza IJ, Malesza M, Walkowiak J, Mussin N, Walkowiak D, Aringazina R, et al. High-fat, western-style diet, systemic inflammation, and gut microbiota: a narrative review. Cells. 2021;10(11):3164,1-31.DOI: 10.3390/cells10113164.

Thomas MS, Blesso CN, Calle MC, Chun OK, Puglisi M, Fernandez ML. Dietary influences on gut microbiota with a focus on metabolic syndrome. Metab Syndr Relat Disord. 2022;20(8):429-439.DOI: 10.1089/met.2021.0131.

Yang J, Wei H, Zhou Y, Szeto CH, Li C, Lin Y, et al. High-fat diet promotes colorectal tumorigenesis through modulating gut microbiota and metabolites. Gastroenterology. 2021;162(1):135-149.DOI: 10.1053/j.gastro.2021.08.041.

Li J, Wu H, Liu Y, Yang L. High-fat diet-induced obesity model using four strains of mice: kunming, C57BL/6, BALB/c and ICR. Exp Anim. 2020;69(3):326-335.DOI: 10.1538/expanim.19-0148.

Tanes C, Bittinger K, Gao Y, Friedman ES, Nessel L, Paladhi UR, et al. Role of dietary fiber in the recovery of the human gut microbiome and its metabolome. Cell Host Microbe. 2021;29(3):394-407.DOI: 10.1016/j.chom.2020.12.012.

Santoso P, Maliza R, Rahayu R, Astrina Y, Syukri F, Maharani S. Extracted yam bean (Pachyrhizus erosus (L.) Urb.) fiber counteracts adiposity, insulin resistance, and inflammation while modulating gut microbiota composition in mice fed with a high-fat diet. Res Pharm Sci. 2022;17(5):558-571.DOI: 10.4103/1735-5362.355213.

Dong Y, Li Q, Guo Y, Zhao Y, Cao J. Comparison of physicochemical and in vitro hypoglycemic activity of bamboo shoot dietary fibers from different regions of Yunnan. Front Nutr. 2023;9:1102671,1-11.DOI: 10.3389/fnut.2022.1102671.

Rebello CJ, O'Neil CE, Greenway FL. Dietary fiber and satiety: the effects of oats on satiety. Nutr Rev. 2016;74(2):131-147.DOI: 10.1093/nutrit/nuv063.

Hijová E, Bertková I, Štofilová J. Dietary fibre as prebiotics in nutrition. Cent Eur J Public Health. 2019;27(3):251-255.DOI: 10.21101/cejph.a5313.

Ho HVT, Sievenpiper JL, Zurbau A, Blanco MS, Jovanovski E, Au-Yeung F, et al. The effect of oat β-glucan on LDL-cholesterol, non-HDL-cholesterol and apoB for CVD risk reduction: a systematic review and meta-analysis of randomised-controlled trials. Br J Nutr. 2016;116(8):1369-1382.DOI: 10.1017/S000711451600341X.

Surampudi P, Enkhmaa B, Anuurad E, Berglund L. Lipid lowering with soluble dietary fiber. Curr Atheroscler Rep. 2016;18(12):75,1-13.DOI: 10.1007/s11883-016-0624-z.

Powthong P, Jantrapanukorn B, Suntornthiticharoen P, Luprasong C. An in vitro study on the effects of selected natural dietary fiber from salad vegetables for lowering intestinal glucose and lipid absorption. Recent Pat Food Nutr Agric. 2021;12(2):123-133.DOI: 10.2174/2212798412666210311163258.

Cronin P, Joyce SA, O'Toole PW, O'Connor EM. Dietary fibre modulates the gut microbiota. Nutrients. 2021;13(5):1655,1-22.DOI: 10.3390/nu13051655.

Xu C, Cheng C, Zhang X, Peng J. Inclusion of soluble fiber in the gestation diet changes the gut microbiota, affects plasma propionate and odd-chain fatty acids levels, and improves insulin sensitivity in sows. Int J Mol Sci. 2020;21(2):635,1-14.DOI: 10.3390/ijms21020635.

Lattimer JM, Haub MD. Effects of dietary fiber and its components on metabolic health. Nutrients. 2010; 2(12):1266-1289.DOI: 10.3390/nu2121266.

Kumalasari ID, Nishi K, Harmayani E, Raharjo S, Sugahara T. Immunomodulatory activity of bengkoang (Pachyrhizus erosus) fiber extract in vitro and in vivo. Cytotechnology. 2014;66(1):75-85.

DOI: 10.1007/s10616-013-9539-5.

Almeida-Suhett CP, Scott JM, Graham A, Chen Y, Deuster PA. Control diet in a high-fat diet study in mice: regular chow and purified low-fat diet have similar effects on phenotypic, metabolic, and behavioral outcomes. Nutr Neurosci. 2019;22(1):19-28.DOI: 10.1080/1028415X.2017.1349359.

Yao L, Wei J, Shi S, Guo K, Wang X, Wang Q, et al. Modified lingguizhugan decoction incorporated with dietary restriction and exercise ameliorates hyperglycemia, hyperlipidemia and hypertension in a rat model of the metabolic syndrome. BMC Complement Altern Med. 2017;17(1):132,1-12.DOI: 10.1186/s12906-017-1557-y.

Ding S, Jiang J, Yu P, Zhang G, Zhang G, Liu X. Green tea polyphenol treatment attenuates atherosclerosis in high-fat diet-fed apolipoprotein E-knockout mice via alleviating dyslipidemia and up-regulating autophagy. PLoS One. 2017;12(8):e0181666,1-18.DOI: 10.1371/journal.pone.0181666.

Li X, Guo J, Ji K, Zhang P. Bamboo shoot fiber prevents obesity in mice by modulating the gut microbiota. Sci Rep. 2016;6(1):32953,1-11.DOI: 10.1038/srep32953.

Qiu M, Jin XY, Zhang CJ, Zhang C, Wang M, Lu YB, et al. Effect of Canna edulis type 3 resistant starch in reducing body weight, serum lipid and acute toxicity. Chinese J Exp Trad Med Form. 2019;24:149-156.DOI: 10.13422/j.cnki.syfjx.20190130.

Praseptiangga D, Wandasari, Widyaastuti D. Chemical and physical properties of canna (Canna edulis) and jack bean (Canavalia ensiformis)-based composite flours. Food Res. 2022;6(2):354-367.DOI: 10.26656/fr.2017.6(2).292.

Harmayani E, Kumalasari ID, Marsono Y. Effect of arrowroot (Maranta arundinacea L.) diet on the selected bacterial population and chemical properties of caecal digesta of Sprague Dawley rats. Int Res J Microbiol. 2011;2:278-284.

Zhang Q, Ke Y, Hong H. HDL and lipid metabolism. Adv Exp Med Biol. 2022;1377:49-61.DOI: 10.1007/978-981-19-1592-5_4.

Santoso P, Maliza R, Insani SJ, Fadhilah Q, Rahayu R. Preventive effect of jicama (Pachyrhizus erosus) fiber against diabetes development in mice fed with high-fat diet. J Appl Pharm Sci. 2021;11(1):137-143.DOI: 10.7324/JAPS.2021.110116.

Novitasari D, Sunarti S, Fatmawati A. Garut chips (Maranta arundinacea Linn) as snacks and blood glucose levels, plasma angiotensin II and blood pressure in patients with type 2 diabetes mellitus (DMT2). Med Medika Indonesiana. 2011;45(1):53-58.

Zhang C, Ma S, Wu J, Luo L, Qiao S, Li R, et al. A specific gut microbiota and metabolomic profiles shifts related to antidiabetic action: the similar and complementary antidiabetic properties of type 3 resistant starch from Canna edulis and metformin. Pharmacol Res. 2020;159:104985,1-41.DOI: 10.1016/j.phrs.2020.104985.

Richards P, Pais R, Habib AM, Brighton CA, Yeo GS, Reimann F, et al. Highfat diet impairs the function of glucagon-like peptide-1 producing L-cells. Peptides. 2016;277:21-27.DOI: 10.1016/j.peptides.2015.06.006.

Nygaard EB, Møller CL, Kievit P, Grove KL, Andersen B. Increased fibroblast growth factor 21 expression in high-fat diet-sensitive non-human primates (Macaca mulatta). Int J Obes (Lond). 2014;38(2):183-191.DOI: 10.1038/ijo.2013.79.

Suzuki S, Aoe S. High β-Glucan barley supplementation improves glucose tolerance by increasing GLP-1 secretion in diet-induced obesity mice. Nutrients. 2021;13(2):527,1-11.DOI: 10.3390/nu13020527.

Martin A, Ecklu-Mensah G, Ha CWY, Hendrick G, Layman DK, Gilbert J, et al. Gut microbiota mediate the FGF21 adaptive stress response to chronic dietary protein-restriction in mice. Nat Commun. 2021;12(1):3838,1-11.DOI: 10.1038/s41467-021-24074-z.

Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature .2012;490(7418):55-60.DOI: 10.1038/nature11450.

Zhai X, Lin D, Zhao Y, Li W, Yang X. Effects of dietary fiber supplementation on fatty acid metabolism and intestinal microbiota diversity in C57BL/6J mice fed with a high-fat diet. J Agric Food Chem. 2018;66(48):12706-12718.DOI: 10.1021/acs.jafc.8b05036.

Lin YC, Lin HF, Wu CC, Chen CL, Ni YH. Pathogenic effects of Desulfovibrio in the gut on fatty liver in diet-induced obese mice and children with obesity. J Gastroenterol. 2018;57(11):913-925.DOI: 10.1007/s00535-022-01909-0.

Shahi SK, Ghimire S, Lehman P, Mangalam AK. Obesity induced gut dysbiosis contributes to disease severity in an animal model of multiple sclerosis. Front Immunol. 2022;3:966417,1-13.DOI: 10.3389/fimmu.2022.966417.

Frappier M, Auclair J, Bouasker S, Gunaratnam S, Diarra C, Millette M. Screening and characterization of some lactobacillaceae for detection of cholesterol-lowering activities. Probiotics Antimicrob Proteins. 2022;14(5):873-883.DOI: 10.1007/s12602-022-09959-9.

Liu HY, Roos S, Jonsson H, Ahl D, Dicksved J, Lindberg JE, et al. Effects of Lactobacillus johnsonii and Lactobacillus reuteri on gut barrier function and heat shock proteins in intestinal porcine epithelial cells. Physiol Rep. 2015;3(4):e12355,1-13.DOI: 10.14814/phy2.12355.

Hu J, Deng F, Zhao B, Lin Z, Sun Q, Yang X, et al. Lactobacillus murinus alleviate intestinal ischemia/reperfusion injury through promoting the release of interleukin-10 from M2 macrophages via Toll-like receptor 2 signaling. Microbiome. 2022;10(1):38,1-21.DOI: 10.1186/s40168-022-01227-w.

Xu J, Liang R, Zhang W, Tian K, Li J, Chen X, et al. Faecalibacterium prausnitzii-derived microbial anti-inflammatory molecule regulates intestinal integrity in diabetes mellitus mice via modulating tight junction protein expression. J Diabetes. 2020;12(3):224-236.DOI: 10.1111/1753-0407.12986.

Lin SJ, Helm ET, Gabler NK, Burrough ER. Acute infection with Brachyspira hyodysenteriae affects mucin expression, glycosylation, and fecal MUC5AC. Front Cell Infect Microbiol. 2023;12:1042815,1-18.DOI: 10.3389/fcimb.2022.1042815.

Herp S, Durai Raj AC, Salvado SM, Woelfel S, Stecher B. The human symbiont Mucispirillum schaedleri: causality in health and disease. Med Microbiol Immunol. 2021;210(4):173-179.DOI: 10.1007/s00430-021-00702-9.

Ussar S, Griffin NW, Bezy O, Fujisaka S, Vienberg S, Softic S, et al. Interactions between gut microbiota, host genetics and diet modulate the predisposition to obesity and metabolic syndrome. Cell Metab. 2015;22(3): 516-530.DOI: 10.1016/j.cmet.2015.07.007.

Tanaka M, Koida A, Miyazaki A, Tabata K, Takei Y, Tanimoto Y, et al. Canna starch improves immune functions and the intestinal environment in mice. Biosci Microbiota Food Health. 2023;42(2):131-137.DOI: 10.12938/bmfh.2022-068.

Rodríguez-Daza MC, Pulido-Mateos EC, Lupien-Meilleur J, Guyonnet D, Desjardins Y, Roy D. Polyphenol-mediated gut microbiota modulation: toward prebiotics and further. Front Nutr. 2021;8:689456,1-24.DOI: 10.3389/fnut.2021.689456.


Refbacks

  • There are currently no refbacks.


Creative Commons LicenseThis work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License which allows users to read, copy, distribute and make derivative works for non-commercial purposes from the material, as long as the author of the original work is cited properly.