Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-05-05T14:49:36.160Z Has data issue: false hasContentIssue false

Macauba (Acrocomia aculeata) pulp oil has the potential to enhance the intestinal barrier morphology, goblet cell proliferation and gut microbiota composition in mice fed a high-fat diet

Published online by Cambridge University Press:  13 November 2023

Cíntia Tomaz Sant’ Ana
Affiliation:
Department of Food Technology, Federal University of Viçosa, Viçosa, MG 36570-000, Brazil
Thaísa Agrizzi Verediano
Affiliation:
Department of Nutrition and Health, Federal University of Viçosa, Viçosa, MG, Brazil
Mariana Grancieri
Affiliation:
Department of Nutrition and Health, Federal University of Viçosa, Viçosa, MG, Brazil
Renata Celi Lopes Toledo
Affiliation:
Department of Nutrition and Health, Federal University of Viçosa, Viçosa, MG, Brazil
Neuza Maria Brunoro Costa
Affiliation:
Department of Pharmacy and Nutrition, Federal University of Espírito Santo, Alegre, ES, Brazil
Hércia Stampini Duarte Martino
Affiliation:
Department of Nutrition and Health, Federal University of Viçosa, Viçosa, MG, Brazil
Frederico Augusto Ribeiro de Barros*
Affiliation:
Department of Food Technology, Federal University of Viçosa, Viçosa, MG 36570-000, Brazil
*
*Corresponding author: Frederico Augusto Ribeiro de Barros, email fredbarros@ufv.br

Abstract

Macauba (Acrocomia aculeata) is a palm tree native from Brazil, whose pulp is rich in oil that has a high content of oleic acid and carotenoids. Macauba pulp oil can bring health benefits due to its bioactive compounds; however, its effects on gut health are unknown. Thus, the objective of this study was to evaluate the effect of macauba pulp oil on the intestinal health in mice fed a high-fat (HF) diet. Male C57BL1/6 mice were randomly divided into three groups (10 animals/group): control diet, HF diet and HF diet with 4 % of macauba pulp oil (HFM). Concentration of short-chain fatty acids (SCFA), faecal pH and histomorphometric analysis of the colon were performed. Content of colon samples was used on microbiome analysis using 16S rRNA amplicon sequencing. Animals from the HFM group had higher butyric acid content and goblet cells number, greater circular and longitudinal muscle layer and higher α-diversity compared with the HF group. Moreover, consumption of MPO reduced Desulfobacterota phylum, Ruminococcaceae, Oscillospiraceae, Prevotellaceae, Bifidobacteriaceae family, Faecalibacterium, Prevotella, Ruminococcus and Enterorhabdus genus. Therefore, macauba pulp oil was able to modulate the gut microbiota and enhance intestinal barrier morphology, showing preventive effects on gut dysbiosis in mice fed a HF diet.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Carbone, E, D‘Amato, P, Vicchio, G, et al. (2021) A systematic review on the role of microbiota in the pathogenesis and treatment of eating disorders. Eur Psychiatry 64, 1.CrossRefGoogle Scholar
Li, L, Zhang, Y, Speakman, JR, et al. (2021) The gut microbiota and its products: establishing causal relationships with obesity related outcomes. Obes Rev 22, e13341.CrossRefGoogle ScholarPubMed
Caruso, R, Lo, BC & Nunez, G (2020) Host–microbiota interactions in inflammatory bowel disease. Nat Rev Immunol 20, 411426.CrossRefGoogle ScholarPubMed
Cunningham, AL, Stephens, JW & Harris, DA (2021) A review on gut microbiota: a central factor in the pathophysiology of obesity. Lipids Health Dis 20, 65.CrossRefGoogle ScholarPubMed
Rinninella, E, Cintoni, M, Raoul, P, et al. (2019) Food components and dietary habits: keys for a healthy gut microbiota composition. Nutrients 11, 2393.CrossRefGoogle ScholarPubMed
Wisniewski, P, Dowden, RA & Campbell, SC (2018) Role of dietary lipids in modulating inflammation through the gut microbiota. Nutrients 11, 117.CrossRefGoogle Scholar
Lyu, Y, Wu, L, Wang, F, et al. (2018) Carotenoid supplementation and retinoic acid in immunoglobulin A regulation of the gut microbiota dysbiosis. Exp Biol Med 243, 613620.CrossRefGoogle ScholarPubMed
Hegde, PS, Agni, MB, Rai, P, et al. (2022) Impact of carotenoids on gut microbiome: implications in human health and disease. J Appl Nat Sci 14, 10851099.Google Scholar
Ciconini, G, Favaro, SP, Roscoe, R, et al. (2013) Biometry and oil contents of Acrocomia aculeata fruits from the Cerrados and Pantanal biomes in Mato Grosso do Sul, Brazil. Ind Crops Prod 45, 208214.CrossRefGoogle Scholar
Coimbra, MC & Jorge, N (2012) Fatty acids and bioactive compounds of the pulps and kernels of Brasilian palm species, guariroba (Syagrus oleracea), jerivá (Syagrus romanzoffiana) and macaúba (Acrocomia aculeata). J Sci Food Agric 92, 679684.CrossRefGoogle Scholar
Sant‘ Ana, CT, Verediano, TA, Grancieri, M, et al. (2023) Macauba (Acrocomia aculeata) pulp oil prevents adipogenesis, inflammation and oxidative stress in mice fed a high-fat diet . Nutrients 15, 1252.CrossRefGoogle ScholarPubMed
Pinheiro-Sant’ana, HM, Stringheta, PC, Brandão, SCC, et al. (1998) Carotenoid retention and vitamin A value in carrot (Daucus carota L.) prepared by food service. Food Chem 61, 145151.CrossRefGoogle Scholar
Rodriguez-Amaya, DBA (2001) A Guide to Carotenoid Analysis in Foods. Washington, DC: ILSI Press.Google Scholar
Ichihara, K & Fukubayashi, Y (2010) Preparation of fatty acid methyl esters for gas-liquid chromatography. J Lipid Res 51, 635640.CrossRefGoogle ScholarPubMed
Percie du Sert, N, Hurst, V, Ahluwalia, A, et al. (2020) The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biol 18, 7.Google ScholarPubMed
Schoemaker, MH, Kleemann, R, Morrison, MC, et al. (2017) A casein hydrolysate based formulation attenuates obesity and associated non-alcoholic fatty liver disease and atherosclerosis in LDLr-/- Leiden mice. PLOS ONE 12, e0180648.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH & Fahey, GC (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123, 19391951.CrossRefGoogle Scholar
Verediano, TA, Viana, ML, Vaz Tostes, MG, et al. (2020) Yacon (Smallanthus sonchifolius) prevented inflammation, oxidative stress, and intestinal alterations in an animal model of colorectal carcinogenesis. J Sci Food Agric 100, 54425449.CrossRefGoogle Scholar
Siegfried, BR, Ruckemann, H & Stumpf, G (1984) Method for the determination of organic acids in silage by high performance liquid chromatography. Landwirtsch Forsch 37, 298304.Google Scholar
Liu, T, Song, X, Na, Y, et al. (2021) Lactobacillus rhamnosus GG colonization in early life ameliorates inflammation of offspring by activating SIRT1/AMPK/PGV-1α pathway. Oxid Med Cell Longev 2021, 3328505.CrossRefGoogle ScholarPubMed
Stevenson, DM & Weimer, PJ (2007) Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl Microbiol Biotechnol 75, 165174.CrossRefGoogle ScholarPubMed
Caporaso, JG, Lauber, CL, Walters, WA, et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6, 16211624.CrossRefGoogle ScholarPubMed
Edgar, RC, Haas, BJ, Clemente, JC, et al. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 21942200.CrossRefGoogle ScholarPubMed
Quast, C, Pruesse, E, Yilmaz, P, et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41, 590596.CrossRefGoogle ScholarPubMed
Douglas, GM, Maffei, VJ, Zaneveld, JR, et al. (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38, 685688.CrossRefGoogle ScholarPubMed
Blankenberg, D, Kuster, G, Coraor, N, et al. (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 19, 121.Google Scholar
Zaunschirm, M, Pignitter, M, Kienesberger, J, et al. (2018) Contribution of the ratio of tocopherol homologs to the oxidative stability of commercial vegetable oils. Molecules 23, 206.CrossRefGoogle Scholar
Venegas, DP, De la Fuente, MK, Landskron, G, et al. (2019) Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol 10, 277.CrossRefGoogle Scholar
Blaak, EE, Canfora, EE, Theis, S, et al. (2020) Short chain fatty acids in human gut and metabolic health. Benef Microbes 11, 411455.CrossRefGoogle ScholarPubMed
Portincasa, P, Bonfrate, L, Vacca, M, et al. (2022) Gut microbiota and short chain fatty acids: implications in glucose homeostasis. Int J Mol Sci 23, 1105.CrossRefGoogle ScholarPubMed
Reboul, E (2019) Mechanisms of carotenoids intestinal absorption: where do we stand? Nutrients 11, 838.CrossRefGoogle ScholarPubMed
Shen, W, Gaskins, HR & McIntosh, MK (2014) Influence of dietary fat on intestinal microbes, inflammation, barrier function and metabolic outcomes. J Nutr Biochem 25, 270280.CrossRefGoogle ScholarPubMed
Stolfi, C, Maresca, C, Monteleone, G, et al. (2022) Implication of intestinal barrier dysfunction in gut dysbiosis and diseases. Biomedicines 10, 2.CrossRefGoogle ScholarPubMed
Yang, S & Yu, M (2021) Role of goblet cells in intestinal barrier and mucosal immunity. J Inflamm Res 13, 31713183.CrossRefGoogle Scholar
Gong, D, Gong, X, Wang, L, et al. (2016) Involvement of reduced microbial diversity in inflammatory bowel disease. Gastroenterol Res Pract 2016, 695109.CrossRefGoogle ScholarPubMed
Lopez-Salazar, V, Tapia, MS, Tobon-Cornejo, S, et al. (2021) Consumption of soybean or olive oil at recommended concentrations increased the intestinal microbiota diversity and insulin sensitivity and prevented fatty liver compared to the effects of coconut oil. J Nutr Biochem 94, 108751.CrossRefGoogle ScholarPubMed
Carbonero, F, Benefiel, AC, Alizadeh-Ghamsari, AH, et al. (2012) Microbial pathways in colonic sulfur metabolism and links with health and disease. Front Physiol 28, 3.Google Scholar
Magne, F, Gotteland, M, Gauthier, L, et al. (2020) The firmicutes/bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients? Nutrients 12, 5.CrossRefGoogle ScholarPubMed
Vital, M, Karch, A & Pieper, DH (2017) Colonic butyrate-producing communities in humans: an overview using omics data. mSystems 2, e00130.CrossRefGoogle ScholarPubMed
Precup, G & Vodnar, DC (2019) Gut Prevotella as a possible biomarker of diet and its eubiotic versus dysbiotic roles: a comprehensive literature review. Br J Nutr 122, 131140.CrossRefGoogle ScholarPubMed
Haro, C, Garcia-Carpintero, S, Rangel-Zuniga, OA, et al. (2017) Consumption of two healthy dietary patterns restored microbiota dysbiosis in obese patients with metabolic dysfunction. Mol Nutr Food Res 61, 12.CrossRefGoogle ScholarPubMed
Graziani, F, Pujol, A, Nicoletti, C, et al. (2016) Ruminococcus gnavus E1 modulates mucin expression and intestinal glycosylation. J Appl Microbiol 120, 14031417.CrossRefGoogle ScholarPubMed
Knudsen, KEB, Laerke, HN, Hedemann, MS, et al. (2018) Impact of diet-modulated butyrate production on intestinal barriers function and inflammation. Nutrients 10, 1499.CrossRefGoogle Scholar
Liu, H, Wang, J, He, T, et al. (2018) Butyrate: a double-edged sword for health? Adv Nutr 9, 2129.CrossRefGoogle ScholarPubMed
Segura Munoz, RR, Mantz, S, Martínez, I, et al. (2022) Experimental evaluation of ecological principles to understand and modulate the outcome of bacterial strain competition in gut microbiomes. ISME J 16, 15941604.CrossRefGoogle ScholarPubMed
US Food and Drug Administration (2005) Estimating the Maximum Safe Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers. Rockville, MD: US Food and Drug Administration.Google Scholar
Elmeliegy, M, Udata, C, Liao, K, et al. (2021) Considerations on the calculation of the human equivalent dose from toxicology studies. Clin Pharmacokinet 60, 563567.CrossRefGoogle ScholarPubMed
Supplementary material: File

Sant’ Ana et al. supplementary material

Sant’ Ana et al. supplementary material
Download Sant’ Ana et al. supplementary material(File)
File 144 KB