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Current Vascular Pharmacology

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ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

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Review Article

Endothelial and Cardiac Dysfunction in Inflammatory Bowel Diseases: Does Treatment Modify the Inflammatory Load on Arterial and Cardiac Structure and Function?

Author(s): Charilaos Triantafyllou *, Maria Nikolaou, Ignatios Ikonomidis, Giorgos Bamias and Ioannis Papaconstantinou

Volume 18, Issue 1, 2020

Page: [27 - 37] Pages: 11

DOI: 10.2174/1570161117666181129095941

Price: $65

Abstract

Inflammatory bowel diseases (IBD), largely represented by Crohn’s disease (CD) and ulcerative colitis (UC), alter gastrointestinal physiology and mucosal immunity through a complex inflammatory process. These diseases can lead to significant arterial endothelial dysfunction. There is also evidence linking IBD with a modification of cardiac structure and function. A growing body of research has associated IBD with an acceleration of arterial stiffness and atherosclerosis and an increased risk of cardiovascular (CV) morbidity and mortality. The focus of this review is two-fold. Firstly, the literature on IBD in relation to CV dysfunction was evaluated (mainly based on 25 relevant surveys carried out between 2005 and 2018). The vast majority of these studies support a significant association of IBD with a deterioration in CV function. Secondly, the literature available regarding the effect of IBD treatment on CV dysfunction was considered based on studies published between 2007 and 2018. This literature search suggests that IBD treatment may have the potential to ameliorate CV dysfunction resulting in CV benefits. This review will analyse the literature as well as consider emerging research perspectives regarding how IBD treatment could improve CV dysfunction.

Keywords: Inflammatory bowel disease, Crohn's disease, ulcerative colitis, inflammation, endothelial dysfunction, atherosclerosis, endothelial glycocalyx, arterial stiffness.

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[1]
Cromer WE, Mathis JM, Granger DN, Chaitanya GV, Alexander JS. Role of the endothelium in inflammatory bowel diseases. World J Gastroenterol 2011; 17(5): 578-93.
[2]
Zanoli L, Rastelli S, Inserra G, Castellino P. Arterial structure and function in inflammatory bowel disease. World J Gastroenterol 2015; 21(40): 11304-11.
[3]
Cibor D, Domagala-Rodacka R, Rodacka T, Jurczyszyn A, Mach T, Owczarek D. Endothelial dysfunction in inflammatory bowel diseases: Pathogenesis, assessment and implications. World J Gastroenterol 2016; 22(3): 1067-77.
[4]
Aslan AN, Sarı C, Özer Sarı S, et al. Association between aortic stiffness and left ventricular function in inflammatory bowel disease. Cardiol J 2016; 23(2): 202-10.
[5]
Caliskan Z, Keles N, Gokturk HS, et al. Is activation in inflammatory bowel diseases associated with further impairment of coronary microcirculation? Int J Cardiol 2016; 223: 176-81.
[6]
Kivrak T, Sunbul M, Cincin A, et al. Two-dimensional speckle tracking echocardiography is useful in early detection of left ventricular impairment in patients with Crohn’s disease. Eur Rev Med Pharmacol Sci 2016; 20(15): 3249-54.
[7]
Deanfield J, Donald A, Ferri C, et al. Endothelial function and dysfunction. Part I: Methodological issues for assessment in the different vascular beds: A statement by the working group on endothelin and endothelial factors of the European society of hypertension. J Hypertens 2005; 23(1): 7-17.
[8]
Corretti MC, Anderson TJ, Benjamin EJ, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: A report of the international brachial artery reactivity task force. J Am Coll Cardiol 2002; 39(2): 257-65.
[9]
Lekakis J, Abraham P, Balbarini A, et al. Methods for evaluating endothelial function: A position statement from the European society of cardiology working group on peripheral circulation. Eur J Cardiovasc Prev Rehabil 2011; 18(6): 775-89.
[10]
Steyers CM 3rd, Miller FJ Jr. Endothelial dysfunction in chronic inflammatory diseases. Int J Mol Sci 2014; 15(7): 11324-49.
[11]
Vlachopoulos C, Xaplanteris P, Aboyans V, et al. The role of vascular biomarkers for primary and secondary prevention. A position paper from the European society of cardiology working group on peripheral circulation: Endorsed by the association for research into arterial structure and physiology (ARTERY) Society. Atherosclerosis 2015; 241(2): 507-32.
[12]
Mattace-Raco F, Hofman A, Verwoert GC, et al. Determinants of pulse wave velocity in healthy people and in the presence of cardiovascular risk factors: Establishing normal and reference values. Eur Heart J 2010; 31(19): 2338-50.
[13]
Alkan E, Karakaş MS, Yıldırım B. Evaluation of increased subclinical atherosclerosis risk with carotid intima-media thickness and pulse wave velocity in inflammatory bowel disease. Turk J Gastroenterol 2014; 25(Suppl. 1): 20-5.
[14]
Aytaç E, Büyüktaş D, Baysal B, et al. Visual evoked potentials and pulse wave velocity in inflammatory bowel disease. Turk J Gastroenterol 2015; 26(1): 15-9.
[15]
Ikonomidis I, Makavos G, Lekakis J. Arterial stiffness and coronary artery disease. Curr Opin Cardiol 2015; 30(4): 422-31.
[16]
Ozturk K, Guler AK, Cakir M, et al. Pulse wave velocity, intima media thickness, and flow-mediated dilatation in patients with normotensive normoglycemic inflammatory bowel disease. Inflamm Bowel Dis 2015; 21(6): 1314-20.
[17]
Pereira T, Correia C, Cardoso J. Novel methods for pulse wave velocity measurement. J Med Biol Eng 2015; 35(5): 555-65.
[18]
Principi M, Mastrolonardo M, Scicchitano P, et al. Endothelial function and cardiovascular risk in active inflammatory bowel diseases. J Crohn’s Colitis 2013; 7(10): 427-33.
[19]
Zanoli L, Boutouyrie P, Fatuzzo P, et al. Inflammation and aortic stiffness: An individual participant data meta-analysis in patients with inflammatory bowel disease. J Am Heart Assoc 2017; 6(10)pii: e007003
[20]
Zanoli L, Cannavò M, Rastelli S, et al. Arterial stiffness is increased in patients with inflammatory bowel disease. J Hypertens 2012; 30(9): 1775-81.
[21]
Zanoli L, Rastelli S, Inserra G, et al. Increased arterial stiffness in inflammatory bowel diseases is dependent upon inflammation and reduced by immunomodulatory drugs. Atherosclerosis 2014; 234(2): 346-51.
[22]
Caliskan Z, Keles N, Kahraman R, et al. Impaired retrobulbar blood flow and increased carotid IMT in patients with Crohn’s disease. Int J Cardiovasc Imaging 2016; 32(11): 1617-23.
[23]
Simova I. Intima-media thickness: Appropriate evaluation and proper measurement, described. Euro Soc Cardio 2015; 13(21): 2-14.
[24]
Becker BE, Chappell D, Bruegger D, Annecke T, Jacob M. Therapeutic strategies targeting the endothelial glycocalyx: Acute deficits, but great potential. Cardiovasc Res 2010; 87(2): 300-10.
[25]
Becker BF, Chappell D, Jacob M. Endothelial glycocalyx and coronary vascular permeability: The fringe benefit. Basic Res Cardiol 2010; 105(6): 687-701.
[26]
Broekhuizen LN, Mooij HL, Kastelein JJ, Stroes ES, Vink H, Nieuwdorp M. Endothelial glycocalyx as potential diagnostic and therapeutic target in cardiovascular disease. Curr Opin Lipidol 2009; 20(1): 57-62.
[27]
Chappell D, Westphal M, Jacob M. The impact of the glycocalyx on microcirculatory oxygen distribution in critical illness. Curr Opin Anaesthesiol 2009; 22(2): 155-62.
[28]
Ikonomidis I, Pavlidis G, Lambadiari V, et al. Early detection of left ventricular dysfunction in first-degree relatives of diabetic patients by myocardial deformation imaging: The role of endothelial glycocalyx damage. Int J Cardiol 2017; 233: 105-12.
[29]
Ikonomidis I, Voumvourakis A, Makavos G, et al. Association of impaired endothelial glycocalyx with arterial stiffness, coronary microcirculatory dysfunction, and abnormal myocardial deformation in untreated hypertensives. J Clin Hypertens (Greenwich) 2018; 20(4): 672-9.
[30]
Kolářová H, Ambrůzová B, Svihálková Šindlerová L, Klinke A, Kubala L. Modulation of endothelial glycocalyx structure under inflammatory conditions. Mediators Inflamm 2014; 2014694312
[31]
Lipowsky HH. Protease activity and the role of the endothelial glycocalyx in inflammation. Drug Discov Today Dis Models 2011; 8(1): 57-62.
[32]
Mulivor AW, Lipowsky HH. Inflammation- and ischemia-induced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol 2004; 286(5): 1672-80.
[33]
van Golen RF, van Gulik TM, Heger M. Mechanistic overview of reactive species-induced degradation of the endothelial glycocalyx during hepatic ischemia/reperfusion injury. Free Radic Biol Med 2012; 52(8): 1382-402.
[34]
Papa A, Santoliquido A, Danese S, et al. Increased carotid intima-media thickness in patients with inflammatory bowel disease. Aliment Pharmacol Ther 2005; 22(9): 839-46.
[35]
Roifman I, Sun YC, Fedwick JP, et al. Evidence of endothelial dysfunction in patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2009; 7(2): 175-82.
[36]
Principi M, Montenegro L, Losurdo G, et al. Endothelial function and cardiovascular risk in patients with inflammatory bowel disease in remission phase. Scand J Gastroenterol 2016; 51(2): 253-5.
[37]
Akdoğan RA, Durakoğlugil ME, Kocaman SA, et al. Increased pulse wave velocity and carotid intima-media thickness in patients with ulcerative colitis. Dig Dis Sci 2013; 58(8): 2293-300.
[38]
Theocharidou E, Gossios TD, Griva T, et al. Is there an association between inflammatory bowel diseases and carotid intima-media thickness? Preliminary data. Angiology 2014; 65(6): 543-50.
[39]
Bernstein CN, Wajda A, Blanchard JF. The incidence of arterial thromboembolic diseases in inflammatory bowel disease: A population-based study. Clin Gastroenterol Hepatol 2008; 6(1): 41-5.
[40]
Haapamäki J, Roine RP, Turunen U, Färkkilä MA, Arkkila PE. Increased risk for coronary heart disease, asthma, and connective tissue diseases in inflammatory bowel disease. J Crohn’s Colitis 2011; 5(1): 41-7.
[41]
Yarur AJ, Deshpande AR, Pechman DM, Tamariz L, Abreu MT, Sussman DA. Inflammatory bowel disease is associated with an increased incidence of cardiovascular events. Am J Gastroenterol 2011; 106(4): 741-7.
[42]
Kristensen SL, Ahlehoff O, Lindhardsen J, et al. Disease activity in inflammatory bowel disease is associated with increased risk of myocardial infarction, stroke and cardiovascular death--a Danish nationwide cohort study. PLoS One 2013; 8(2)e56944
[43]
Kristensen SL, Ahlehoff O, Lindhardsen J, et al. Inflammatory bowel disease is associated with an increased risk of hospitalization for heart failure: A Danish nationwide cohort study. Circ Heart Fail 2014; 7(5): 717-22.
[44]
Prijić R, Premužić V, Brinar M, Krznarić Ž, Jelaković B, Čuković-Čavka S. Increased arterial stiffness - similar findings in patients with inflammatory bowel disease without prior hypertension or diabetes and in patients with well-controlled hypertension. Blood Press 2018; 27(4): 240-6.
[45]
Cappello M, Licata A, Calvaruso V, et al. Increased expression of markers of early atherosclerosis in patients with inflammatory bowel disease. Eur J Intern Med 2017; 37: 83-9.
[46]
Gomollón F, Dignass A, Annese V, et al. Third European evidence-based consensus on the diagnosis and management of crohn’s disease 2016: Part 1: Diagnosis and medical management. J Crohn’s Colitis 2017; 11(1): 3-25.
[47]
Harbord M, Eliakim R, Bettenworth D, et al. Third European evidence-based consensus on diagnosis and management of ulcerative colitis. part 2: Current Management. J Crohn’s Colitis 2017; 11(7): 769-84.
[48]
Dorn SD, Sandler RS. Inflammatory bowel disease is not a risk factor for cardiovascular disease mortality: Results from a systematic review and meta-analysis. Am J Gastroenterol 2007; 102(3): 662-7.
[49]
Sridhar AR, Parasa S, Navaneethan U, Crowell MD, Olden K. Comprehensive study of cardiovascular morbidity in hospitalized inflammatory bowel disease patients. J Crohn’s Colitis 2011; 5(4): 287-94.
[50]
Ruisi P, Makaryus JN, Ruisi M, Makaryus AN. Inflammatory bowel disease as a risk factor for premature coronary artery disease. J Clin Med Res 2015; 7(4): 257-61.
[51]
Schinzari F, Armuzzi A, De Pascalis B, et al. Tumor necrosis factor-alpha antagonism improves endothelial dysfunction in patients with Crohn’s disease. Clin Pharmacol Ther 2008; 83(1): 70-6.
[52]
Altorjay I, Veréb Z, Serfozo Z, et al. Anti-TNF-alpha antibody (infliximab) therapy supports the recovery of eNOS and VEGFR2 protein expression in endothelial cells. Int J Immunopathol Pharmacol 2011; 24(2): 323-35.
[53]
Rutella S, Fiorino G, Vetrano S, et al. Infliximab therapy inhibits inflammation-induced angiogenesis in the mucosa of patients with Crohn’s disease. Am J Gastroenterol 2011; 106(4): 762-70.
[54]
Kitai T, Kirsop J, Tang WH. Exploring the microbiome in heart failure. Curr Heart Fail Rep 2016; 13(2): 103-9.
[55]
Lau K, Srivatsav V, Rizwan A, et al. Bridging the gap between gut microbial dysbiosis and cardiovascular diseases. Nutrients 2017; 9(8)pii: E859
[56]
Nagatomo Y, Tang WH. Intersections between microbiome and heart failure: Revisiting the gut hypothesis. J Card Fail 2015; 21(12): 973-80.
[57]
Schiattarella GG, Sannino A, Esposito G, Perrino C. Diagnostics and therapeutic implications of gut microbiota alterations in cardiometabolic diseases. Trends Cardiovasc Med 2019; 29(3): 141-7.
[58]
Trøseid M, Ueland T, Hov JR, et al. Microbiota-dependent metabolite trimethylamine-N-oxide is associated with disease severity and survival of patients with chronic heart failure. J Intern Med 2015; 277(6): 717-26.
[59]
Tang WH, Wang Z, Fan Y, et al. Prognostic value of elevated levels of intestinal microbe-generated metabolite trimethylamine-N-oxide in patients with heart failure: Refining the gut hypothesis. J Am Coll Cardiol 2014; 64(18): 1908-14.
[60]
Tang WH, Kitai T, Hazen SL. Gut microbiota in cardiovascular health and disease. Circ Res 2017; 120(7): 1183-96.
[61]
Suzuki T, Heaney LM, Bhandari SS, Jones DJ, Ng LL. Trimethylamine N-oxide and prognosis in acute heart failure. Heart 2016; 102(11): 841-8.
[62]
Tang WH, Wang Z, Shrestha K, et al. Intestinal microbiota-dependent phosphatidylcholine metabolites, diastolic dysfunction, and adverse clinical outcomes in chronic systolic heart failure. J Card Fail 2015; 21(2): 91-6.
[63]
Organ CL, Otsuka H, Brushan S, et al. Choline diet and its gut microbe-derived metabolite, trimethylamine n-oxide, exacerbate pressure overload-induced heart failure. Circ Heart Fail 2016; 9(1)e002314
[64]
Li Z, Wu Z, Yan J, et al. Gut microbe-derived metabolite trimethylamine N-oxide induces cardiac hypertrophy and fibrosis. Lab Invest 2019; 99(3): 346-57.
[65]
Afsar B, Takir M, Kostek O, Covic A, Kanbay M. Endocan: A new molecule playing a role in the development of hypertension and chronic kidney disease? J Clin Hypertens (Greenwich) 2014; 16(12): 914-6.
[66]
Balta S, Mikhailidis DP, Demirkol S, Ozturk C, Celik T, Iyisoy A. Endocan: A novel inflammatory indicator in cardiovascular disease? Atherosclerosis 2015; 243(1): 339-43.
[67]
Cox LA, van Eijk LT, Ramakers BP, et al. Inflammation-induced increases in plasma endocan levels are associated with endothelial dysfunction in humans in vivo. Shock 2015; 43(4): 322-6.
[68]
Arman Y, Akpinar TS, Kose M, et al. Effect of glycemic regulation on endocan levels in patients with diabetes: a preliminary study. Angiology 2016; 67(3): 239-44.
[69]
Lv Y, Zhang Y, Shi W, et al. The association between endocan levels and subclinical atherosclerosis in patients with type 2 diabetes mellitus. Am J Med Sci 2017; 353(5): 433-8.
[70]
Qiu C, Sui J, Zhang Q, Wei P, Wang P, Fu Q. Relationship of endothelial cell-specific molecule 1 level in stress hyperglycemia patients with acute ST-segment elevation myocardial infarction: A pilot study. Angiology 2016; 67(9): 829-34.
[71]
Balta S, Mikhailidis DP, Demirkol S, et al. Endocan--a novel inflammatory indicator in newly diagnosed patients with hypertension: A pilot study. Angiology 2014; 65(9): 773-7.
[72]
Celik T, Balta S, Karaman M, et al. Endocan, a novel marker of endothelial dysfunction in patients with essential hypertension: Comparative effects of amlodipine and valsartan. Blood Press 2015; 24(1): 55-60.
[73]
Cimen T, Efe TH, Akyel A, et al. Human endothelial cell-specific molecule-1 (Endocan) and coronary artery disease and microvascular angina. Angiology 2016; 67(9): 846-53.
[74]
Kose M, Emet S, Akpinar TS, et al. Serum endocan level and the severity of coronary artery disease: A pilot study. Angiology 2015; 66(8): 727-31.
[75]
Wang XS, Yang W, Luo T, Wang JM, Jing YY. Serum endocan levels are correlated with the presence and severity of coronary artery disease in patients with hypertension. Genet Test Mol Biomarkers 2015; 19(3): 124-7.
[76]
Xiong C, Zhao ZW, Chen ZY, et al. Elevated human endothelial cell-specific molecule-1 level and its association with coronary artery disease in patients with hypertension. J Investig Med 2015; 63(7): 867-70.
[77]
Turan T, Akyuz AR, Aykan AC, et al. Plasma endocan levels in patients with isolated coronary artery ectasia. Angiology 2016; 67(10): 932-6.
[78]
Kundi H, Gok M, Kiziltunc E, et al. The relationship between serum endocan levels with the presence of slow coronary flow: A cross-sectional study. Clin Appl Thromb Hemost 2017; 23(5): 472-7.
[79]
Ye MF, Zhao ZW, Luo YK, Dong XF, Yan YM. Elevated endocan concentration is associated with coronary slow flow. Scand J Clin Lab Invest 2016; 76(5): 345-8.
[80]
Voiosu T, Balanescu P, Bengus A, et al. Serum endocan levels are increased in patients with inflammatory bowel disease. Clin Lab 2014; 60(3): 505-10.
[81]
Bu J, Wang Z. Cross-talk between gut microbiota and heart via the routes of metabolite and immunity. Gastroenterol Res Pract 2018; 20186458094
[82]
DiRienzo DB. Effect of probiotics on biomarkers of cardiovascular disease: Implications for heart-healthy diets. Nutr Rev 2014; 72(1): 18-29.
[83]
Ebel B, Lemetais G, Beney L, et al. Impact of probiotics on risk factors for cardiovascular diseases. A review. Crit Rev Food Sci Nutr 2014; 54(2): 175-89.
[84]
Miglioranza Scavuzzi B, Miglioranza LH, Henrique FC, et al. The role of probiotics on each component of the metabolic syndrome and other cardiovascular risks. Expert Opin Ther Targets 2015; 19(8): 1127-38.
[85]
Sun J, Buys N. Effects of probiotics consumption on lowering lipids and CVD risk factors: A systematic review and meta-analysis of randomized controlled trials. Ann Med 2015; 47(6): 430-40.
[86]
Thushara RM, Gangadaran S, Solati Z, Moghadasian MH. Cardiovascular benefits of probiotics: A review of experimental and clinical studies. Food Funct 2016; 7(2): 632-42.
[87]
Wang L, Guo MJ, Gao Q, et al. The effects of probiotics on total cholesterol: A meta-analysis of randomized controlled trials. Medicine (Baltimore) 2018; 97(5)e9679
[88]
Aihara K, Kajimoto O, Hirata H, Takahashi R, Nakamura Y. Effect of powdered fermented milk with Lactobacillus helveticus on subjects with high-normal blood pressure or mild hypertension. J Am Coll Nutr 2005; 24(4): 257-65.
[89]
Barreto FM, Colado Simao AN, Morimoto HK, et al. Beneficial effects of Lactobacillus plantarum on glycemia and homocysteine levels in postmenopausal women with metabolic syndrome. Nutrition 2014; 30(7-8): 939-42.
[90]
Bayat A, Azizi-Soleiman F, Heidari-Beni M, et al. Effect of cucurbita ficifolia and probiotic yogurt consumption on blood glucose, lipid profile, and inflammatory marker in type 2 diabetes. Int J Prev Med 2016; 7: 30.
[91]
Chen Y, Liu W, Xue J, et al. Angiotensin-converting enzyme inhibitory activity of Lactobacillus helveticus strains from traditional fermented dairy foods and antihypertensive effect of fermented milk of strain H9. J Dairy Sci 2014; 97(11): 6680-92.
[92]
Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V. Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition 2012; 28(5): 539-43.
[93]
Firouzi S, Majid HA, Ismail A, Kamaruddin NA, Barakatun-Nisak MY. Effect of multi-strain probiotics (multi-strain microbial cell preparation) on glycemic control and other diabetes-related outcomes in people with type 2 diabetes: A randomized controlled trial. Eur J Nutr 2017; 56(4): 1535-50.
[94]
Fuentes MC, Lajo T, Carrion JM, Cune J. Cholesterol-lowering efficacy of Lactobacillus plantarum CECT 7527, 7528 and 7529 in hypercholesterolaemic adults. Br J Nutr 2013; 109(10): 1866-72.
[95]
Jones ML, Martoni CJ, Parent M, Prakash S. Cholesterol-lowering efficacy of a microencapsulated bile salt hydrolase-active Lactobacillus reuteri NCIMB 30242 yoghurt formulation in hypercholesterolaemic adults. Br J Nutr 2012; 107(10): 1505-13.
[96]
Kadooka Y, Sato M, Imaizumi K, et al. Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 2010; 64(6): 636-43.
[97]
Kiessling G, Schneider J, Jahreis G. Long-term consumption of fermented dairy products over 6 months increases HDL cholesterol. Eur J Clin Nutr 2002; 56(9): 843-9.
[98]
Moroti C, Souza Magri LF, de Rezende Costa M, Cavallini DC, Sivieri K. 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.
[99]
Ostadrahimi A, Taghizadeh A, Mobasseri M, et al. Effect of probiotic fermented milk (kefir) on glycemic control and lipid profile in type 2 diabetic patients: A randomized double-blind placebo-controlled clinical trial. Iran J Public Health 2015; 44(2): 228-37.
[100]
Savcheniuk OA, Virchenko OV, Falalyeyeva TM, et al. The efficacy of probiotics for monosodium glutamate-induced obesity: Dietology concerns and opportunities for prevention. EPMA J 2014; 5(1): 2.
[101]
Shakeri H, Hadaegh H, Abedi F, et al. Consumption of synbiotic bread decreases triacylglycerol and vldl levels while increasing HDL levels in serum from patients with type-2 diabetes. Lipids 2014; 49(7): 695-701.
[102]
Stenman LK, Waget A, Garret C, et al. Probiotic B420 and prebiotic polydextrose improve efficacy of antidiabetic drugs in mice. Diabetol Metab Syndr 2015; 7: 75.
[103]
Tonucci LB, Olbrich Dos Santos KM, Licursi de Oliveira L, Rocha Ribeiro SM, Duarte Martino HS. Clinical application of probiotics in type 2 diabetes mellitus: A randomized, double-blind, placebo-controlled study. Clin Nutr 2017; 36(1): 85-92.
[104]
Tsai TY, Chen LY, Pan TM. Effect of probiotic-fermented, genetically modified soy milk on hypercholesterolemia in hamsters. J Microbiol Immunol Infect 2014; 47(1): 1-8.
[105]
Celiberto LS, Bedani R, Rossi EA, Cavallini DC. Probiotics: The scientific evidence in the context of inflammatory bowel disease. Crit Rev Food Sci Nutr 2017; 57(9): 1759-68.
[106]
Eom T, Kim YS, Choi CH, Sadowsky MJ, Unno T. Current understanding of microbiota- and dietary-therapies for treating inflammatory bowel disease. J Microbiol 2018; 56(3): 189-98.
[107]
Wasilewski A, Zielińska M, Storr M, Fichna J. Beneficial effects of probiotics, prebiotics, synbiotics, and psychobiotics in inflammatory bowel disease. Inflamm Bowel Dis 2015; 21(7): 1674-82.
[108]
Derwa Y, Gracie DJ, Hamlin PJ, Ford AC. Systematic review with meta-analysis: the efficacy of probiotics in inflammatory bowel disease. Aliment Pharmacol Ther 2017; 46(4): 389-400.
[109]
Parker EA, Roy T, D’Adamo CR, Wieland LS. Probiotics and gastrointestinal conditions: An overview of evidence from the cochrane collaboration. Nutrition 2018; 45: 125-34.
[110]
Rondanelli M, Faliva MA, Perna S, Giacosa A, Peroni G, Castellazzi AM. Using probiotics in clinical practice: Where are we now? A review of existing meta-analyses. Gut Microbes 2017; 8(6): 521-43.

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