Effects of enriched seafood sticks (heat-inactivated B. animalis subsp. lactis CECT 8145, inulin, omega-3) on cardiometabolic risk factors and gut microbiota in abdominally obese subjects: randomized controlled trial

Judit Companys, Lorena Calderón-Pérez, Laura Pla-Pagà, Elisabet Llauradó, Berner Andrée Sandoval-Ramirez, Maria José Gosalbes, Ainara Arregui, Maddi Barandiaran, Antoni Caimari, Josep Maria Del Bas, Lluís Arola, Rosa M Valls, Rosa Solà, Anna Pedret, Judit Companys, Lorena Calderón-Pérez, Laura Pla-Pagà, Elisabet Llauradó, Berner Andrée Sandoval-Ramirez, Maria José Gosalbes, Ainara Arregui, Maddi Barandiaran, Antoni Caimari, Josep Maria Del Bas, Lluís Arola, Rosa M Valls, Rosa Solà, Anna Pedret

Abstract

Purpose: To assess the effects of enriched seafood sticks with postbiotic and bioactive compounds on CMD risk factors and the gut microbiota in abdominally obese individuals.

Methods: Randomized, double-blind, parallel, placebo-controlled trial with abdominally obese individuals. Participants (n = 120) consumed 50 g/day of enriched seafood sticks containing SIAP: (1010 colony forming units (CFUs) of heat-inactivated B. animalis subsp. lactis CECT8145, 370 mg/day omega 3 and 1.7 g/day inulin), or 50 g/day of placebo seafood sticks for 12 weeks. At 12 weeks, an acute single-dose study of 4 h was performed.

Results: Sustained SIAP2 consumption significantly decreased the insulin by - 5.25 mg/dL and HOMA-IR (homeostatic Model Assessment of Insulin Resistance) by - 1.33. In women, SIAP2 consumption significantly decreased the pulse pressure (PP) by - 4.69 mmHg. Gut microbiota analysis showed a negative association between glycemic parameter reduction and Alistipes finegoldii and Ruminococcaceae, and between PP reduction and Prevotella 9-ASV0283 and Christensenellaceae. In the acute single dose-study 4-h, SIAP2 consumption produced a lower increase in the postprandial circulating triglyceride levels [23.9 (7.03) mg/dL (mean [standard error])] than the observed with placebo [49.0 (9.52)] mg/dL.

Conclusion: In abdominally obese individuals, enriched seafood sticks induce a potential protection against type 2 diabetes development by the reduction in the insulin and HOMA-IR; and in cardiovascular disease, in women, by the PP reduction. These effects are accompanied by partial changes in the gut microbiota composition. The enriched seafood sticks reduce the atherogenic triglyceride postprandial concentrations. Our results support the use of enriched seafood sticks as a complementary strategy in the management of CMD risk factors. REGISTRATION NUMBER OF CLINICAL TRIAL: ( www.

Clinicaltrials: gov ): NCT03630588 (August 15, 2018).

Keywords: Cardiometabolic disease; Gut microbiota; Inulin; Omega 3; Postbiotics; Type 2 diabetes management.

Conflict of interest statement

The authors A.A. and M.B. employees of Angulas Aguinaga Research Center and played no role in any result or conclusion. For all other authors, no competing financial interests exist.

© 2022. The Author(s).

Figures

Fig. 1
Fig. 1
Flowchart of the participant study
Fig. 2
Fig. 2
(A) Comparison of gut microbiota α-diversity indexes between both group of intervention (Placebo and SIAP2) at baseline and after 12 weeks of intervention: (A.1) diversity differences (Shannon index), (A.2) richness differences (Chao 1 index). p < 0.05 for intra-treatment comparisons. #p < 0.02 for inter-treatment comparisons at 12 weeks of intervention (vs. Placebo); (B) Principal coordinates analysis (PCoA) based on Bray–Curtis dissimilarity index. (C) Linear discriminant analysis effect size (LEfSe) describing the differences between bacterial groups in abdominally obese subjects before (baseline) and after consuming SIAP2 for 12 weeks (LDA score > 2.0). (D) Relevant associations network, between clinical parameters that observed significant changes after 12 weeks of SIAP2 treatment and gut microbiota, at ASV level (r > 0.5) performed using a multivariant method (sparce partial least square). *Color lines show the correlation between ASVs and clinical variables. The positive and negative associations were related with line colors (association index)

References

    1. World Health Organization (2016) Cardiovascular diseases (CVDs) fact sheets. In: World Health Organisation.
    1. Attaye I, Pinto-Sietsma S-J, Herrema H, Nieuwdorp M. A crucial role for diet in the relationship between gut microbiota and cardiometabolic disease. Annu Rev Med. 2020;71:149–161. doi: 10.1146/annurev-med-062218-023720.
    1. Ross R, Neeland IJ, Yamashita S, et al. Waist circumference as a vital sign in clinical practice: a Consensus Statement from the IAS and ICCR Working Group on Visceral Obesity. Nat Rev Endocrinol. 2020;16:177–189. doi: 10.1038/s41574-019-0310-7.
    1. Sangrós FJ, Torrecilla J, Giráldez-García C, et al. Association of general and abdominal obesity with hypertension, dyslipidemia and prediabetes in the PREDAPS study. Rev Española Cardiol. 2018;71:170–177. doi: 10.1016/j.rec.2017.04.035.
    1. Orio F, Muscogiuri G, Nese C, et al. Obesity, type 2 diabetes mellitus and cardiovascular disease risk: an uptodate in the management of polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol. 2016;207:214–219. doi: 10.1016/j.ejogrb.2016.08.026.
    1. Thomas F, Pannier B, Bean K, Danchin N. Waist circumference and mortality: impact of associated risk factors. Diabetes Metab. 2011;37:33–38. doi: 10.1016/j.diabet.2010.07.003.
    1. FAO/WHO (2002) Guidelines for the evaluation of probiotics in food (Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food)
    1. Companys J, Pla-Pagà L, Calderón-Pérez L, et al. Fermented dairy products, probiotic supplementation, and cardiometabolic diseases: a systematic review and meta-analysis. Adv Nutr. 2020;11:834–863. doi: 10.1093/advances/nmaa030.
    1. Caimari A, del Bas JM, Boqué N, et al. Heat-killed Bifidobacterium animalis subsp. Lactis CECT 8145 increases lean mass and ameliorates metabolic syndrome in cafeteria-fed obese rats. J Funct Foods. 2017;38:251–263. doi: 10.1016/j.jff.2017.09.029.
    1. Żółkiewicz J, Marzec A, Ruszczyński M, Feleszko W. Postbiotics—a step beyond pre- and probiotics. Nutrients. 2020;12:2189. doi: 10.3390/nu12082189.
    1. Pedret A, Valls RM, Calderón-Pérez L, et al (2019) Effects of daily consumption of the probiotic Bifidobacterium animalis subsp. lactis CECT 8145 on anthropometric adiposity biomarkers in abdominally obese subjects: a randomized controlled trial. Int J Obes. 10.1038/s41366-018-0220-0
    1. Piqué N, Berlanga M, Miñana-Galbis D. Health benefits of heat-killed (tyndallized) probiotics: an overview. Int J Mol Sci. 2019;20:2534. doi: 10.3390/ijms20102534.
    1. Nataraj BH, Ali SA, Behare PV, Yadav H. Postbiotics-parabiotics: the new horizons in microbial biotherapy and functional foods. Microb Cell Fact. 2020;19:1–22. doi: 10.1186/S12934-020-01426-W/TABLES/2.
    1. Wu Y, Zhang Q, Ren Y, Ruan Z. Effect of probiotic Lactobacillus on lipid profile: a systematic review and meta-analysis of randomized, controlled trials. PLoS ONE. 2017;12:e0178868. doi: 10.1371/journal.pone.0178868.
    1. Rajkumar H, Mahmood N, Kumar M, et al. Effect of probiotic (VSL#3) and omega-3 on lipid profile, insulin sensitivity, inflammatory markers, and gut colonization in overweight adults: a randomized. Controlled Trial Mediators Inflamm. 2014;2014:348959. doi: 10.1155/2014/348959.
    1. European Commission (2006) Database of health claims submitted to EFSA for evaluation
    1. Tada H, Takamura M, Kawashiri Maki (2020) Genomics of hypertriglyceridemia, 1st edn. Elsevier, Amsterdam
    1. Companys J, Pla-Pagà L, Calderón-Pérez L, et al. Fermented dairy products, probiotic supplementation, and cardiometabolic diseases: a systematic review and meta-analysis. Adv Nutr. 2020 doi: 10.1093/advances/nmaa030.
    1. Dunn AB, Hanson L, Vandevusse L, Leslie S. Through the microbial looking glass: premature labor, preeclampsia, and gestational diabetes: a scoping review. J Perinat Neonatal Nurs. 2019;33:35–51. doi: 10.1097/JPN.0000000000000375.
    1. Wegh G, Knol,, et al. Postbiotics and their potential applications in early life nutrition and beyond. Int J Mol Sci. 2019;20:4673. doi: 10.3390/ijms20194673.
    1. Piepoli MF, Hoes AW, Agewall S, et al. 2016 European guidelines on cardiovascular disease prevention in clinical practice. Eur Heart J. 2016;37:2315–2381. doi: 10.1093/eurheartj/ehw106.
    1. Cortés B, Núñez I, Cofán M, et al. Acute effects of high-fat meals enriched with walnuts or olive oil on postprandial endothelial function. J Am Coll Cardiol. 2006;48:1666–1671. doi: 10.1016/j.jacc.2006.06.057.
    1. Van Der Kooy K, Leenen R, Seidell JC, et al. Abdominal diameters as indicators of visceral fat: comparison between magnetic resonance imaging and anthropometry. Br J Nutr. 1993;70:47–58. doi: 10.1079/BJN19930104.
    1. Kadooka Y, Sato M, Ogawa A, et al. Effect of Lactobacillus gasseri SBT2055 in fermented milk on abdominal adiposity in adults in a randomised controlled trial. Br J Nutr. 2013 doi: 10.1017/S0007114513001037.
    1. Schaudinn A, Linder N, Garnov N, et al. Predictive accuracy of single- and multi-slice MRI for the estimation of total visceral adipose tissue in overweight to severely obese patients. NMR Biomed. 2015;28:583–590. doi: 10.1002/nbm.3286.
    1. Siu AL, Bibbins-Domingo K, Grossman D, et al. Screening for high blood pressure in adults: U.S. preventive services task force recommendation statement. Ann Intern Med. 2015;163:778–786. doi: 10.7326/M15-2223.
    1. Expert Panel on Detection, Evaluation and T of HBC in A (2001) Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA J Am Med Assoc 285:2486–2497. 10.1001/jama.285.19.2486
    1. Farrán A, Zamora R, Cervera P (2004) Tablas de composición de alimentos del Cesnid
    1. Vallbona C, Roure C, Violan F, Alegre M (2007) Guia de prescripció d’exercici físic per a la salut (PEFS). Dirección General de Salud Pública y Secretaría General del Deporte (Departamento de la Vicepresidencia), Generalitat de Catalunya
    1. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27:863–864. doi: 10.1093/bioinformatics/btr026.
    1. R Core Team (2020) R: A language and environment for statistical computing. R A Lang. Environ. Stat. Comput. R Found. Stat. Comput. Vienna, Austria
    1. Callahan BJ, McMurdie PJ, Rosen MJ, et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869.
    1. Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D596. doi: 10.1093/nar/gks1219.
    1. Rohart F, Gautier B, Singh A, Lê Cao K-A. mixOmics: an R package for ‘omics feature selection and multiple data integration. PLOS Comput Biol. 2017;13:e1005752. doi: 10.1371/journal.pcbi.1005752.
    1. Ekhlasi G, Zarrati M, Agah S, et al (2017) Effects of symbiotic and vitamin E supplementation on blood pressure, nitric oxide and inflammatory factors in non-alcoholic fatty liver disease. EXCLI J 16:278–290. 10.17179/excli2016-846
    1. Harbaoui B, Nanchen D, Lantelme P, et al. Prognostic value of pulse pressure after an acute coronary syndrome. Atherosclerosis. 2018;277:219–226. doi: 10.1016/j.atherosclerosis.2018.07.013.
    1. Tajabadi-Ebrahimi M, Sharifi N, Farrokhian A, et al. A randomized controlled clinical trial investigating the effect of synbiotic administration on markers of insulin metabolism and lipid profiles in overweight type 2 diabetic patients with coronary heart disease. Exp Clin Endocrinol Diabetes. 2017;125:21–27. doi: 10.1055/s-0042-105441.
    1. Pedret A, Valls RM, Calderón-Pérez L, et al. Effects of daily consumption of the probiotic Bifidobacterium animalis subsp. lactis CECT 8145 on anthropometric adiposity biomarkers in abdominally obese subjects: a randomized controlled trial. Int J Obes. 2019;43:1863–1868. doi: 10.1038/s41366-018-0220-0.
    1. Taubert D, Roesen R, Lehmann C, et al. Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide: a randomized controlled trial. JAMA. 2007;298:49–60. doi: 10.1001/JAMA.298.1.49.
    1. Solà R, Valls RM, Godàs G, et al. Cocoa, hazelnuts, sterols and soluble fiber cream reduces lipids and inflammation biomarkers in hypertensive patients: a randomized controlled trial. PLoS ONE. 2012 doi: 10.1371/JOURNAL.PONE.0031103.
    1. Sergeev IN, Aljutaily T, Walton G, Huarte E. Effects of synbiotic supplement on human gut microbiota, body composition and weight loss in obesity. Nutrients. 2020 doi: 10.3390/NU12010222.
    1. Borgeraas H, Johnson LK, Skattebu J, et al. Effects of probiotics on body weight, body mass index, fat mass and fat percentage in subjects with overweight or obesity: a systematic review and meta-analysis of randomized controlled trials. Obes Rev. 2018;19:219–232. doi: 10.1111/obr.12626.
    1. Moroti C, Souza Magri LF, de Rezende CM, et al. Effect of the consumption of a new symbiotic shake on glycemia and cholesterol levels in elderly people with type 2 diabetes mellitus. Lipids Health Dis. 2012;11:29. doi: 10.1186/1476-511X-11-29.
    1. O’Mahoney LL, Matu J, Price OJ, et al. Omega-3 polyunsaturated fatty acids favourably modulate cardiometabolic biomarkers in type 2 diabetes: a meta-analysis and meta-regression of randomized controlled trials. Cardiovasc Diabetol. 2018;17:98. doi: 10.1186/s12933-018-0740-x.
    1. Cotillard A, Kennedy SP, Kong LC, et al (2013) Erratum: Dietary intervention impact on gut microbial gene richness (Nature (2013) 500 (585–588). 10.1038/nature12480). Nature
    1. Ravachol J, De Philip P, Borne R, et al. Mechanisms involved in xyloglucan catabolism by the cellulosome-producing bacterium Ruminiclostridium cellulolyticum. Sci Rep. 2016;6:1–17. doi: 10.1038/srep22770.
    1. Precup G, Vodnar D-C. Gut Prevotella as a possible biomarker of diet and its eubiotic versus dysbiotic roles: a comprehensive literature review. Br J Nutr. 2019;122:131–140. doi: 10.1017/S0007114519000680.
    1. Zagato E, Pozzi C, Bertocchi A, et al. Endogenous murine microbiota member Faecalibaculum rodentium and its human homologue protect from intestinal tumour growth. Nat Microbiol. 2020;5:511–524. doi: 10.1038/s41564-019-0649-5.
    1. Chambers ES, Viardot A, Psichas A, et al. Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut. 2015;64:1744–1754. doi: 10.1136/gutjnl-2014-307913.
    1. Gomez-Arango LF, Barrett HL, McIntyre HD, et al. Increased systolic and diastolic blood pressure is associated with altered gut microbiota composition and butyrate production in early pregnancy. Hypertension. 2016;68:974–981. doi: 10.1161/HYPERTENSIONAHA.116.07910.
    1. Jie Z, Bang-yao L, Ming-jie X, et al. Studies on the effects of polydextrose intake on physiologic functions in Chinese people. Am J Clin Nutr. 2000;72:1503–1509. doi: 10.1093/ajcn/72.6.1503.
    1. Modica S, Gadaleta RM, Moschetta A (2010) Deciphering the nuclear bile acid receptor FXR paradigm. Nucl Recept Signal 8:nrs.08005. 10.1621/nrs.08005
    1. Vaarala O. Gut microbiota and type 1 diabetes. Rev Diabet Stud. 2012;9:251–259. doi: 10.1900/RDS.2012.9.251.

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