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In vitro and animal studies

On the effect of flavonoids and dietary fibre in lingonberries on atherosclerotic plaques, lipid profiles and gut microbiota composition in Apoe–/– mice

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 1080-1090 | Received 26 Apr 2022, Accepted 22 Jul 2022, Published online: 05 Aug 2022

References

  • Aronson D, Burger AJ. 2010. The relationship between transient and persistent worsening renal function and mortality in patients with acute decompensated heart failure. J Card Failure. 16(7):541–547.
  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 7(5):335–336.
  • Carlson JL, Erickson JM, Lloyd BB, Slavin JL. 2018. Health effects and sources of prebiotic dietary fiber. Curr Dev Nutr. 2(3):nzy005.
  • Chen C, You LJ, Huang Q, Fu X, Zhang B, Liu RH, Li C. 2018. Modulation of gut microbiota by mulberry fruit polysaccharide treatment of obese diabetic db/db mice. Food Funct. 9(7):3732–3742.
  • Chen YR, Zheng HM, Zhang GX, Chen FL, Chen LD, Yang ZC. 2020. High Oscillospira abundance indicates constipation and low BMI in the Guangdong Gut Microbiome Project. Sci Rep. 10(1):9364.
  • Collins HL, Drazul-Schrader D, Sulpizio AC, Koster PD, Williamson Y, Adelman SJ, Owen K, Sanli T, Bellamine A. 2016. L-Carnitine intake and high trimethylamine N-oxide plasma levels correlate with low aortic lesions in ApoE(-/-) transgenic mice expressing CETP. Atherosclerosis. 244:29–37.
  • EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA). 2016. Dietary Reference Values for choline. EFSA J. 14(8):4484.
  • Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, et al. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 110(22):9066–9071.
  • Falls JG, Blake BL, Cao Y, Levi PE, Hodgson E. 1995. Gender differences in hepatic expression of flavin-containing monooxygenase isoforms (FMO1, FMO3, and FMO5) in mice. J Biochem Toxicol. 10(3):171–177.
  • Fåk F, Jakobsdottir G, Kulcinskaja E, Marungruang N, Matziouridou C, Nilsson U, Stålbrand H, Nyman M. 2015. The physico-chemical properties of dietary fibre determine metabolic responses, short-chain Fatty Acid profiles and gut microbiota composition in rats fed low- and high-fat diets. PLoS One. 10(5):e0127252.
  • Gregory JC, Buffa JA, Org E, Wang Z, Levison BS, Zhu W, Wagner MA, Bennett BJ, Li L, DiDonato JA, et al. 2015. Transmission of atherosclerosis susceptibility with gut microbial transplantation. J Biol Chem. 290(9):5647–5660.
  • Gui T, Shimokado A, Sun Y, Akasaka T, Muragaki Y. 2012. Diverse roles of macrophages in atherosclerosis: from inflammatory biology to biomarker discovery. Mediators Inflamm. 2012:693083.
  • Hefni ME, Bergström M, Lennqvist T, Fagerström C, Witthöft CM. 2021. Simultaneous quantification of trimethylamine N-oxide, trimethylamine, choline, betaine, creatinine, and propionyl-, acetyl-, and l-carnitine in clinical and food samples using HILIC-LC-MS. Anal Bioanal Chem. 413(21):5349–5360.
  • Henningsson AM, Björck IME, Nyman EMGL. 2002. Combinations of indigestible carbohydrates affect short-chain fatty acid formation in the hindgut of rats. J Nutr. 132(10):3098–3104.
  • Herp S, Durai Raj AC, Salvado Silva M, Woelfel S, Stecher B. 2021. The human symbiont Mucispirillum schaedleri: causality in health and disease. Med Microbiol Immunol. 210(4):173–179.
  • Heyman-Linden L, Kotowska D, Sand E, Bjursell M, Plaza M, Turner C, Holm C, Fåk F, Berger K. 2016. Lingonberries alter the gut microbiota and prevent low-grade inflammation in high-fat diet fed mice. Food Nutr Res. 60:29993.
  • Jakobsdottir G, Xu J, Molin G, Ahrné S, Nyman M. 2013. High-fat diet reduces the formation of butyrate, but increases succinate, inflammation, liver fat and cholesterol in rats, while dietary fibre counteracts these effects. PLoS One. 8(11):e80476.
  • Jones ML, Martoni CJ, Ganopolsky JG, Labbe A, Prakash S. 2014. The human microbiome and bile acid metabolism: dysbiosis, dysmetabolism, disease and intervention. Expert Opin Biol Ther. 14(4):467–482.
  • Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC, Bayless AJ, Wilson KE, Glover LE, Kominsky DJ, Magnuson A, et al. 2015. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe. 17(5):662–671.
  • Koay YC, Chen YC, Wali JA, Luk AWS, Li M, Doma H, Reimark R, Zaldivia MTK, Habtom HT, Franks AE, et al. 2021. Plasma levels of trimethylamine-N-oxide can be increased with ‘healthy’ and ‘unhealthy’ diets and do not correlate with the extent of atherosclerosis but with plaque instability. Cardiovasc Res. 117(2):435–449.
  • Kohsaka S, Jin Z, Rundek T, Homma S, Sacco RL, Di Tullio MR. 2010. Relationship between serum lipid values and atherosclerotic burden in the proximal thoracic aorta. Int J Stroke. 5(4):257–263.
  • Koliada A, Syzenko G, Moseiko V, Budovska L, Puchkov K, Perederiy V, Gavalko Y, Dorofeyev A, Romanenko M, Tkach S, et al. 2017. Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol. 17(1):120.
  • Kriss M, Hazleton KZ, Nusbacher NM, Martin CG, Lozupone CA. 2018. Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery. Curr Opin Microbiol. 44:34–40.
  • Kypreos KE, Karagiannides I, Fotiadou EH, Karavia EA, Brinkmeier MS, Giakoumi SM, Tsompanidi EM. 2009. Mechanisms of obesity and related pathologies: Role of apolipoprotein E in the development of obesity. Febs J. 276(20):5720–5728.
  • Lagkouvardos I, Lesker TR, Hitch TCA, Galvez EJC, Smit N, Neuhaus K, Wang J, Baines JF, Abt B, Stecher B, et al. 2019. Sequence and cultivation study of Muribaculaceae reveals novel species, host preference, and functional potential of this yet undescribed family. Microbiome. 7(1):28.
  • le Roes-Hill M, Khan N, Burton SG. 2011. Actinobacterial peroxidases: an unexplored resource for biocatalysis. Appl Biochem Biotechnol. 164(5):681–713.
  • Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. 2005. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 102(31):11070–11075.
  • Li J, Lin S, Vanhoutte PM, Woo CW, Xu A. 2016. Akkermansia muciniphila protects against atherosclerosis by preventing metabolic endotoxemia-induced inflammation in Apoe-/- mice. Circulation. 133(24):2434–2446.
  • Lindskog Jonsson A, Caesar R, Akrami R, Reinhardt C, Fåk Hållenius F, Borén J, Bäckhed F. 2018. Impact of gut microbiota and diet on the development of atherosclerosis in Apoe-/- mice. Arterioscler Thromb Vasc Biol. 38(10):2318–2326.
  • Liu J, Hefni ME, Witthoft CM. 2020. Characterization of flavonoid compounds in common Swedish berry species. Foods. 9(3):358.
  • Lo Sasso G, Schlage WK, Boue S, Veljkovic E, Peitsch MC, Hoeng J. 2016. The Apoe(-/-) mouse model: a suitable model to study cardiovascular and respiratory diseases in the context of cigarette smoke exposure and harm reduction. J Transl Med. 14(1):146.
  • Ma J, Li H. 2018. The role of gut microbiota in atherosclerosis and hypertension. Front Pharmacol. 9:1082.
  • Madduma Hewage S, Prashar S, O K, Siow YL. 2021. Lingonberry improves non-alcoholic fatty liver disease by reducing hepatic lipid accumulation, oxidative stress and inflammatory response. Antioxidants. 10(4):565.
  • Marungruang N, Kovalenko T, Osadchenko I, Voss U, Huang F, Burleigh S, Ushakova G, Skibo G, Nyman M, Prykhodko O, et al. 2020. Lingonberries and their two separated fractions differently alter the gut microbiota, improve metabolic functions, reduce gut inflammatory properties, and improve brain function in ApoE-/- mice fed high-fat diet. Nutr Neurosci. 23(8):600–612.
  • Matziouridou C, Marungruang N, Nguyen TD, Nyman M, Fåk F. 2016. Lingonberries reduce atherosclerosis in Apoe(-/-) mice in association with altered gut microbiota composition and improved lipid profile. Mol Nutr Food Res. 60(5):1150–1160.
  • Messer JS, Chang EB. 2018. Microbial physiology of the digestive tract and its role in inflammatory bowel diseases. In: Said HM, editor. Physiology of the Gastrointestinal Tract. Cambridge: Academic Press; p. 795–810.
  • Pap N, Fidelis M, Azevedo L, do Carmo MAV, Wang D, Mocan A, Pereira EPR, Xavier-Santos D, Sant’Ana AS, Yang B, et al. 2021. Berry polyphenols and human health: Evidence of antioxidant, anti-inflammatory, microbiota modulation, and cell-protecting effects. Curr Opin Food Sci. 42:167–186.
  • Rafieian-Kopaei M, Setorki M, Doudi M, Baradaran A, Nasri H. 2014. Atherosclerosis: process, indicators, risk factors and new hopes. Int J Prev Med. 5(8):927–946.
  • Rao SSC, Attaluri A, Anderson L, Stumbo P. 2007. Ability of the normal human small intestine to absorb fructose: evaluation by breath testing. Clin Gastroenterol Hepatol. 5(8):959–963.
  • Ravnskov U. 2002. Is atherosclerosis caused by high cholesterol? QJM. 95(6):397–403.
  • Richards LB, Li M, Esch B, Garssen J, Folkerts G. 2016. The effects of short-chain fatty acids on the cardiovascular system. PharmaNutrition. 4(2):68–111.
  • Rodríguez-Daza MC, Roquim M, Dudonné S, Pilon G, Levy E, Marette A, Roy D, Desjardins Y. 2020. Berry polyphenols and fibers modulate distinct microbial metabolic functions and gut microbiota enterotype-like clustering in obese mice. Front Microbiol. 11:2032.
  • Senthong V, Wang Z, Li XS, Fan Y, Wu Y, Tang WH, Hazen SL. 2016. Intestinal microbiota-generated metabolite trimethylamine-N-oxide and 5-year mortality risk in stable coronary artery disease: the contributory role of intestinal microbiota in a COURAGE-like patient cohort. J Am Heart Assoc. 5(6):e002816.
  • Vendrame S, Guglielmetti S, Riso P, Arioli S, Klimis-Zacas D, Porrini M. 2011. Six-week consumption of a wild blueberry powder drink increases Bifidobacteria in the human gut. J Agric Food Chem. 59(24):12815–12820.
  • Vilkickyte G, Raudonis R, Motiekaityte V, Vainoriene R, Burdulis D, Viskelis J, Raudone L. 2019. Composition of sugars in wild and cultivated lingonberries (Vaccinium vitis-idaea L.). Molecules. 24(23):4225.
  • Zhao G, Nyman M, Åke Jönsson J. 2006. Rapid determination of short-chain fatty acids in colonic contents and faeces of humans and rats by acidified water-extraction and direct-injection gas chromatography. Biomed Chromatogr. 20(8):674–682.
  • Zhao S, Liu W, Wang J, Shi J, Sun Y, Wang W, Ning G, Liu R, Hong J. 2017. Akkermansia muciniphila improves metabolic profiles by reducing inflammation in chow diet-fed mice. J Mol Endocrinol. 58(1):1–14.