Effects of sardine-enriched diet on metabolic control, inflammation and gut microbiota in drug-naïve patients with type 2 diabetes: a pilot randomized trial

Mariona Balfegó, Silvia Canivell, Felicia A Hanzu, Aleix Sala-Vila, Margarita Martínez-Medina, Serafín Murillo, Teresa Mur, Elena G Ruano, Francisca Linares, Nuria Porras, Silvia Valladares, Maria Fontalba, Elena Roura, Anna Novials, Cristina Hernández, Gloria Aranda, Antoni Sisó-Almirall, Gemma Rojo-Martínez, Rafael Simó, Ramon Gomis, Mariona Balfegó, Silvia Canivell, Felicia A Hanzu, Aleix Sala-Vila, Margarita Martínez-Medina, Serafín Murillo, Teresa Mur, Elena G Ruano, Francisca Linares, Nuria Porras, Silvia Valladares, Maria Fontalba, Elena Roura, Anna Novials, Cristina Hernández, Gloria Aranda, Antoni Sisó-Almirall, Gemma Rojo-Martínez, Rafael Simó, Ramon Gomis

Abstract

Background: Nutrition therapy is the cornerstone of treating diabetes mellitus. The inclusion of fish (particularly oily fish) at least two times per week is recommended by current international dietary guidelines for type 2 diabetes. In contrast to a large number of human studies examining the effects of oily fish on different cardiovascular risk factors, little research on this topic is available in patients with type 2 diabetes. The aims of this pilot study were to investigate the effects of a sardine-enriched diet on metabolic control, adiponectin, inflammatory markers, erythrocyte membrane fatty acid (EMFA) composition, and gut microbiota in drug-naïve patients with type 2 diabetes.

Methods: 35 drug-naïve patients with type 2 diabetes were randomized to follow either a type 2 diabetes standard diet (control group: CG), or a standard diet enriched with 100 g of sardines 5 days a week (sardine group: SG) for 6 months. Anthropometric, dietary information, fasting glycated hemoglobin, glucose, insulin, adiponectin, inflammatory markers, EMFA and specific bacterial strains were determined before and after intervention.

Results: There were no significant differences in glycemic control between groups at the end of the study. Both groups decreased plasma insulin (SG: -35.3%, P = 0.01, CG: -22.6%, P = 0.02) and homeostasis model of assessment--insulin resistance (HOMA-IR) (SG: -39.2%, P = 0.007, CG: -21.8%, P = 0.04) at 6-months from baseline. However only SG increased adiponectin in plasma compared to baseline level (+40.7%, P = 0.04). The omega-3 index increased 2.6% in the SG compared to 0.6% in the CG (P = 0.001). Both dietary interventions decreased phylum Firmicutes (SG and CG: P = 0.04) and increased E. coli concentrations (SG: P = 0.01, CG: P = 0.03) at the end of the study from baseline, whereas SG decreased Firmicutes/Bacteroidetes ratio (P = 0.04) and increased Bacteroides-Prevotella (P = 0.004) compared to baseline.

Conclusions: Although enriching diet with 100 g of sardines 5 days a week during 6 months to a type 2 diabetes standard diet seems to have neutral effects on glycemic control in drug-naïve patients with type 2 diabetes, this nutritional intervention could have beneficial effects on cardiovascular risk. Furthermore, both dietary interventions decreased HOMA-IR and altered gut microbiota composition of drug-naïve patients with type 2 diabetes.

Trial registration: Trial number and name of the registry: NCT02294526, ClinicalTrials.gov.

Keywords: Nutrition therapy; Oily fish; Pilot trial; Sardine; Type 2 diabetes.

Figures

Fig. 1
Fig. 1
Design of Pilchardus study
Fig. 2
Fig. 2
The CONSORT flow diagram

References

    1. International Diabetes Federation . IDF Diabetes Atlas. 6. Brussels: International Diabetes Federation; 2013.
    1. Evert AB, Boucher JL, Cypress M, Dunbar SA, Franz MJ, Mayer-Davis EJ, et al. Nutrition therapy recommendations for the management of adults with diabetes. Diabetes Care. 2014;37(Suppl 1):S120–43. doi: 10.2337/dc14-S120.
    1. Mann JI, De Leeuw I, Hermansen K, Karamanos B, Karlström B, Katsilambros N, et al. Evidence-based nutritional approaches to the treatment and prevention of diabetes mellitus. Nutr Metab Cardiovasc Dis. 2004;14:373–94. doi: 10.1016/S0939-4753(04)80028-0.
    1. Harris WS. The omega-3 index: clinical utility for therapeutic intervention. Curr Cardiol Rep. 2010;12:503–8. doi: 10.1007/s11886-010-0141-6.
    1. Bosch J, Gerstein HC, Dagenais GR, Díaz R, Dyal L, Jung H, et al. n–3 Fatty Acids and Cardiovascular Outcomes in Patients with Dysglycemia. N Engl J Med. 2012;367:309–18. doi: 10.1056/NEJMoa1203859.
    1. Madani Z, Louchami K, Sener A, Malaisse WJ, Ait YD. Dietary sardine protein lowers insulin resistance, leptin and TNF-α and beneficially affects adipose tissue oxidative stress in rats with fructose-induced metabolic syndrome. Int J Mol Med. 2012;29:311–8.
    1. Mellouk Z, Ait Yahia D, Boukortt F, Benaicha N, Madani Z, Bouchenak M. Dietary sardine (Sardina pilchardus) protein attenuates hyperglycemia and hyperlipidemia and ameliorates tissue morphology changes in streptozotocin-induced diabetic rats. Met Funct Res Diabetes. 2009;2:45–54.
    1. Varela-Moreiras G, Avila JM, Cuadrado C, del Pozo S, Ruiz E, Moreiras O. Evaluation of food consumption and dietary patterns in Spain by the Food Consumption Survey: updated information. Eur J Clin Nutr. 2010;64(Suppl 3):S37–43. doi: 10.1038/ejcn.2010.208.
    1. Tilg H, Moschen AR. Food, immunity, and the microbiome. Gastroenterology. 2015;148:1107–19. doi: 10.1053/j.gastro.2014.12.036.
    1. American Diabetes Association Classification and diagnosis of diabetes. Sec. 2. In Standards of Medical Care in Diabetes. Diabetes Care. 2016;39(Suppl 1):S13–22.
    1. Alicia Foundation. .
    1. Sala-Vila A, Harris WS, Cofán M, Pérez-Heras AM, Pintó X, Lamuela-Raventós RM, et al. Determinants of the omega-3 index in a Mediterranean population at increased risk for CHD. Br J Nutr. 2011;106:425–31. doi: 10.1017/S0007114511000171.
    1. Karlström BE, Järvi AE, Byberg L, Berglund LG, Vessby BOH. Fatty fish in the diet of patients with type 2 diabetes: comparison of the metabolic effects of foods rich in n-3 and n-6 fatty acids. Am J Clin Nutr. 2011;94:26–33. doi: 10.3945/ajcn.110.006221.
    1. Kondo K, Morino K, Nishio Y, Kondo M, Nakao K, Nakagawa F, et al. A fish-based diet intervention improves endothelial function in postmenopausal women with type 2 diabetes mellitus: a randomized crossover trial. Metabolism. 2014;63:930–40. doi: 10.1016/j.metabol.2014.04.005.
    1. Dunstan DW, Mori TA, Puddey IB, Beilin LJ, Burke V, Morton AR, et al. The independent and combined effects of aerobic exercise and dietary fish intake on serum lipids and glycemic control in NIDDM. A randomized controlled study. Diabetes Care. 1997;20:913–21. doi: 10.2337/diacare.20.6.913.
    1. Mori TA, Bao DQ, Burke V, Puddey IB, Watts GF, Beilin LJ. Dietary fish as a major component of a weight-loss diet: effect on serum lipids, glucose, and insulin metabolism in overweight hypertensive subjects. Am J Clin Nutr. 1999;70:817–25.
    1. Ramel A, Martinéz A, Kiely M, Morais G, Bandarra NM, Thorsdottir I. Beneficial effects of long-chain n-3 fatty acids included in an energy-restricted diet on insulin resistance in overweight and obese European young adults. Diabetologia. 2008;51:1261–8. doi: 10.1007/s00125-008-1035-7.
    1. Sallé A, Ryan M, Ritz P. Underreporting of food intake in obese diabetic and nondiabetic patients. Diabetes Care. 2006;29:2726–7. doi: 10.2337/dc06-1582.
    1. Trento M, Passera P, Tomalino M, Bajardi M, Pomero F, Allione A, et al. Group visits improve metabolic control in type 2 diabetes: a 2-year follow-up. Diabetes Care. 2001;24:995–1000. doi: 10.2337/diacare.24.6.995.
    1. Abete I, Parra D, Crujeiras AB, Goyenechea E, Martinez JA. Specific insulin sensitivity and leptin responses to a nutritional treatment of obesity via a combination of energy restriction and fatty fish intake. J Hum Nutr Diet. 2008;21:591–600. doi: 10.1111/j.1365-277X.2008.00902.x.
    1. Navas-Carretero S, Pérez-Granados AM, Schoppen S, Vaquero MP. An oily fish diet increases insulin sensitivity compared to a red meat diet in young iron-deficient women. Br J Nutr. 2009;102:546–53. doi: 10.1017/S0007114509220794.
    1. Hartweg J, Perera R, Montori V, Dinneen S, Neil HAW, Farmer A. Omega-3 polyunsaturated fatty acids (PUFA) for type 2 diabetes mellitus. Cochrane database Syst Rev. 2008;1:CD003205.
    1. Martínez-González MA, Salas-Salvadó J, Estruch R, Corella DD, Fitó M, Ros E. Benefits of the Mediterranean Diet: Insights from the PREDIMED Study. Prog Cardiovasc Dis. 2015;58:50–60. doi: 10.1016/j.pcad.2015.04.003.
    1. Dietary fibre and incidence of type 2 diabetes in eight European countries: the EPIC-InterAct Study and a meta-analysis of prospective studies. Diabetologia. 2015;58:1394–408.
    1. Pereira MA, Jacobs DR, Pins JJ, Raatz SK, Gross MD, Slavin JL, et al. Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults. Am J Clin Nutr. 2002;75:848–55.
    1. Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, Tobe K. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest. 2006;116:1784–92. doi: 10.1172/JCI29126.
    1. Neale EP, Muhlhausler B, Probst YC, Batterham MJ, Fernandez F, Tapsell LC. Short-term effects of fish and fish oil consumption on total and high molecular weight adiponectin levels in overweight and obese adults. Metabolism. 2013;62:651–60. doi: 10.1016/j.metabol.2012.10.014.
    1. Zhang J, Wang C, Li L, Man Q, Meng L, Song P, et al. Dietary inclusion of salmon, herring and pompano as oily fish reduces CVD risk markers in dyslipidaemic middle-aged and elderly Chinese women. Br J Nutr. 2012;108:1455–65. doi: 10.1017/S0007114511006866.
    1. Wu JHY, Cahill LE, Mozaffarian D. Effect of fish oil on circulating adiponectin: a systematic review and meta-analysis of randomized controlled trials. J Clin Endocrinol Metab. 2013;98(6):2451–9. doi: 10.1210/jc.2012-3899.
    1. Rosa FT, Freitas EC, Deminice R, Jordão AA, Marchini JS. Oxidative stress and inflammation in obesity after taurine supplementation: a double-blind, placebo-controlled study. Eur J Nutr. 2014;53:823–30. doi: 10.1007/s00394-013-0586-7.
    1. Jacobs DR, Gross MD, Tapsell LC. Food synergy: an operational concept for understanding nutrition. Am J Clin Nutr. 2009;89(5):1543S–1548S. doi: 10.3945/ajcn.2009.26736B.
    1. Tsitouras PD, Gucciardo F, Salbe AD, Heward C, Harman SM. High omega-3 fat intake improves insulin sensitivity and reduces CRP and IL6, but does not affect other endocrine axes in healthy older adults. Horm Metab Res. 2008;40:199–205. doi: 10.1055/s-2008-1046759.
    1. Cho YI, Mooney MP, Cho DJ. Hemorheological disorders in diabetes mellitus. J Diabetes Sci Technol. 2008;2:1130–8. doi: 10.1177/193229680800200622.
    1. Weijers RNM. Lipid composition of cell membranes and its relevance in type 2 diabetes mellitus. Curr Diabetes Rev. 2012;8:390–400. doi: 10.2174/157339912802083531.
    1. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–23. doi: 10.1038/4441022a.
    1. Furet J-P, Kong L-C, Tap J, Poitou C, Basdevant A, Bouillot J-L, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010;59:3049–57. doi: 10.2337/db10-0253.
    1. Greenhill C. Gut microbiota: Firmicutes and Bacteroidetes involved in insulin resistance by mediating levels of glucagon-like peptide 1. Nat Rev Endocrinol. 2015;11:254. doi: 10.1038/nrendo.2015.40.
    1. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63. doi: 10.1038/nature12820.
    1. Yu H-N, Zhu J, Pan W, Shen S-R, Shan W-G, Das UN. Effects of fish oil with a high content of n-3 polyunsaturated fatty acids on mouse gut microbiota. Arch Med Res. 2014;45:195–202. doi: 10.1016/j.arcmed.2014.03.008.
    1. Andersen AD, Mølbak L, Michaelsen KF, Lauritzen L. Molecular fingerprints of the human fecal microbiota from 9 to 18 months old and the effect of fish oil supplementation. J Pediatr Gastroenterol Nutr. 2011;53:303–9. doi: 10.1097/MPG.0b013e31821d298f.
    1. Nadal I, Santacruz A, Marcos A, Warnberg J, Garagorri JM, Garagorri M, et al. Shifts in clostridia, bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents. Int J Obes. 2009;33:758–67. doi: 10.1038/ijo.2008.260.
    1. Karlsson FH, Tremaroli V, Nookaew I, Bergström G, Behre CJ, Fagerberg B, et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498:99–103. doi: 10.1038/nature12198.
    1. 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;490:55–60. doi: 10.1038/nature11450.

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner