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Effect of Synbiotic and Probiotic Supplementation on Serum Levels of Endothelial Cell Adhesion Molecules in Hemodialysis Patients: a Randomized Control Study

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Abstract

The aim of this study was to investigate the effect of synbiotic and probiotic supplementation on serum vascular dysfunction and necrosis markers in hemodialysis (HD) patients. In this randomized, double-blind, placebo-controlled trial, 75 HD patients were randomly assigned to either the synbiotic or probiotic or placebo group. The patients in the synbiotic group received 15 g of prebiotics and 5 g probiotic powder containing Lactobacillus acidophilus strain T16 (IBRC-M10785), Bifidobacterium bifidum strain BIA-6, Bifidobacterium lactis strain BIA-6, Bifidobacterium longum strain LAF-5 (2.7 × 107 CFU/g each) in sachets (n = 25), whereas the probiotic group received 5 g probiotics same to the first group with 15 g of maltodextrin powder in sachets (n = 25) and the placebo group received 20 g of maltodextrin powder in sachets (n = 25) for 12 weeks. At baseline and the end of the study, serum concentrations of soluble intercellular adhesion molecule type 1 (sICAM-1), soluble vascular cell adhesion molecule type 1 (sVCAM-1), cytokeratin 18 (CK-18) as the necrosis marker, uric acid, and phosphate levels were measured. Feces also were collected for microbiota colony counting. Serum ICAM-1 level reduced significantly in the synbiotic group after the intervention period (P = 0.02), and this reduction was significantly different in the synbiotic group in comparison to the placebo group (P = 0.03). Serum levels of VCAM-1 and CK-18 were not significantly different between the groups. However, the reduction in serum levels of VCAM-1 in the synbiotic group was significantly higher in comparison to the placebo group (P = 0.01). Multivariate linear regression analysis revealed that ∆ phosphate was the sole independent determinant of ∆ICAM-1 (P = 0 < 001). The study indicated that synbiotic supplementation reduced serum ICAM-1 level, which is a risk factor for cardiovascular diseases in HD patients, but has no effect on the necrosis marker. Trial registration: www.irct.ir (IRCT2017041233393N1).

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References

  1. Jungers P, Nguyen Khoa T, Z a M et al (1999) Incidence of atherosclerotic arterial occlusive accidents in predialysis and dialysis patients: a multicentric study in the Ile de France district. Nephrol. Dial. Transplant 14:898–902

    Article  CAS  Google Scholar 

  2. Papagianni A, Kokolina E, Kalovoulos M, Vainas A, Dimitriadis C, Memmos D (2004) Carotid atherosclerosis is associated with inflammation, malnutrition and intercellular adhesion molecule-1 in patients on continuous ambulatory peritoneal dialysis. Nephrol Dial Transplant 19:1258–1263. https://doi.org/10.1093/ndt/gfh078

    Article  CAS  PubMed  Google Scholar 

  3. Canaud B, Cristol JP, Morena M, Leray-Moragues H, Bosc JY, Vaussenat F (1999) Imbalance of oxidants and antioxidants in haemodialysis patients. Blood Purif 17:99–106

    Article  CAS  Google Scholar 

  4. Locatelli F, Canaud B, Eckardt K-U, Stenvinkel P, Wanner C, Zoccali C (2003) Oxidative stress in end-stage renal disease: an emerging threat to patient outcome. Nephrol Dial Transplant 18:1272–1280. https://doi.org/10.1093/ndt/gfg074

    Article  CAS  PubMed  Google Scholar 

  5. Lobo JC, Stockler-Pinto MB, Da Nóbrega ACL et al (2013) Is there association between uric acid and inflammation in hemodialysis patients? Ren Fail 35:361–366. https://doi.org/10.3109/0886022X.2013.764274

    Article  CAS  PubMed  Google Scholar 

  6. Barros AF, Borges NA, Ferreira DC, Carmo FL, Rosado AS, Fouque D, Mafra D (2015) Is there interaction between gut microbial profile and cardiovascular risk in chronic kidney disease patients? Future Microbiol 10:517–526. https://doi.org/10.2217/fmb.14.140

    Article  CAS  PubMed  Google Scholar 

  7. Wang AY-M, Lam CW-K, Wang M, Woo J, Chan IHS, Lui SF, Sanderson JE, Li PKT (2005) Circulating soluble vascular cell adhesion molecule 1: relationships with residual renal function, cardiac hypertrophy, and outcome of peritoneal dialysis patients. Am J Kidney Dis 45:715–729. https://doi.org/10.1053/j.ajkd.2004.12.012

    Article  CAS  PubMed  Google Scholar 

  8. Bonomini M, Reale M, Santarelli P, Stuard S, Settefrati N, Albertazzi A (1998) Serum levels of soluble adhesion molecules in chronic renal failure and dialysis patients. Nephron 79:399–407. https://doi.org/10.1159/000045084

    Article  CAS  PubMed  Google Scholar 

  9. Musial K, Zwolinska D, Polak-Jonkisz D et al (2004) Soluble adhesion molecules in children and young adults on chronic hemodialysis. PediatrNephrol 19:332–336. https://doi.org/10.1007/s00467-003-1353-4

    Article  Google Scholar 

  10. Musial K, Zwolinska D, Berny U et al (2004) Soluble adhesion molecules in children and young adults with chronic renal failure treated conservatively. Rocz Akad Med Bialymst 49:209–212

    CAS  PubMed  Google Scholar 

  11. Musiał K, Zwolińska D, Polak-Jonkisz D, Berny U, Szprynger K, Szczepańska M (2005) Serum VCAM-1, ICAM-1, and L-selectin levels in children and young adults with chronic renal failure. PediatrNephrol 20(1):52–55. https://doi.org/10.1007/s00467-004-1691-x

    Article  Google Scholar 

  12. Bolton CH, Downs LG, Victory JG et al (2001) Endothelial dysfunction in chronic renal failure: roles of lipoprotein oxidation and pro-inflammatory cytokines. Nephrol Dial Transpl 16:1189–1197. https://doi.org/10.1093/ndt/16.6.1189

    Article  CAS  Google Scholar 

  13. Ritz E, Hahn K, Ketteler M, et al (2012) Phosphate additives in food--a health risk. Dtsch {Ä}rzteblatt Int 109:49–55. doi: https://doi.org/10.3238/arztebl.2012.0049

  14. Rahabi-Layachi H, Ourouda R, Boullier A, Massy ZA, Amant C (2015) Distinct effects of inorganic phosphate on cell cycle and apoptosis in human vascular smooth muscle cells. J Cell Physiol 230:347–355. https://doi.org/10.1002/jcp.24715

    Article  CAS  PubMed  Google Scholar 

  15. Vart P, Nigatu YT, Jaglan A, van Zon SKR, Shafique K (2015) Joint effect of hypertension and elevated serum phosphorus on the risk of mortality in National Health and Nutrition Examination Survey-III. J Am Heart Assoc 4(5). https://doi.org/10.1161/JAHA.114.001706

  16. Truong LD, Shen SS, Park MH, Krishnan B (2009) Diagnosing nonneoplastic lesions in nephrectomy specimens. Arch Pathol Lab Med 133:189–200

    PubMed  Google Scholar 

  17. Vaziri ND, Zhao YY, Pahl MV (2016) Altered intestinal microbial flora and impaired epithelial barrier structure and function in CKD: the nature, mechanisms, consequences and potential treatment. Nephrol Dial Transplant 31:737–746. https://doi.org/10.1093/ndt/gfv095

    Article  CAS  PubMed  Google Scholar 

  18. Neto MPC, Aquino JS, da Silva LFR et al (2018) Gut microbiota and probiotics intervention: a potential therapeutic target for management of cardiometabolic disorders and chronic kidney disease? Pharmacol Res 130:152–163. https://doi.org/10.1016/j.phrs.2018.01.020

    Article  CAS  Google Scholar 

  19. Hlivak P, Jahnova E, Odraska J et al (2005) Long-term (56-week) oral administration of probiotic Enterococcus faecium M-74 decreases the expression of sICAM-1 and monocyte CD54, and increases that of lymphocyte CD49d in humans. Hypertension 16(80):11

    Google Scholar 

  20. Angulo S, Llopis M, Antolin M et al (2006) Lactobacillus casei prevents the upregulation of ICAM-1 expression and leukocyte recruitment in experimental colitis. Am J Physiol Gastrointest Liver Physiol 291:G1155–G1162. https://doi.org/10.1152/ajpgi.00446.2005

    Article  CAS  PubMed  Google Scholar 

  21. Chu Z-X, Chen H-Q, Ma Y-L, Zhou YK, Zhang M, Zhang P, Qin HL (2010) Lactobacillus plantarum prevents the upregulation of adhesion molecule expression in an experimental colitis model. Dig Dis Sci 55:2505–2513. https://doi.org/10.1007/s10620-009-1063-2

    Article  CAS  PubMed  Google Scholar 

  22. Kocijancic M, Cubranic Z, Vujicic B, Racki S, Dvornik S, Zaputovic L (2016) Soluble intracellular adhesion molecule-1 and omentin-1 as potential biomarkers of subclinical atherosclerosis in hemodialysis patients. Int Urol Nephrol 48:1145–1154. https://doi.org/10.1007/s11255-016-1275-2

    Article  CAS  PubMed  Google Scholar 

  23. Rabb H, Calderon E, Bittle PA, Ramirez G (1996) Alterations in soluble intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in hemodialysis patients. Am J Kidney Dis 27:239–243. https://doi.org/10.1016/S0272-6386(96)90547-8

    Article  CAS  PubMed  Google Scholar 

  24. Klein A, Vogelsang H, Kuhnt K, Jahreis G (2003) Probiotika und deren Wirkung auf das Immunsystem (probiotics and their effect on the immune system). Proc German Nutr Soc 70:5

    Google Scholar 

  25. Seidel C, Boehm V, Vogelsang H, Wagner A, Persin C, Glei M, Pool-Zobel BL, Jahreis G (2007) Influence of prebiotics and antioxidants in bread on the immune system, antioxidative status and antioxidative capacity in male smokers and non-smokers. Br J Nutr 97:349–356. https://doi.org/10.1017/S0007114507328626

    Article  CAS  PubMed  Google Scholar 

  26. Jahreis G, Vogelsang H, Kiessling G, Schubert R, Bunte C, Hammes WP (2002) Influence of probiotic saucage (Lactobacillus paracasei) on blood lipids and immunological parameters of healthy volunteers. Food Res Int 35:133–138. https://doi.org/10.1016/S0963-9969(01)00174-0

    Article  CAS  Google Scholar 

  27. Soleimani A, Zarrati Mojarrad M, Bahmani F, Taghizadeh M, Ramezani M, Tajabadi-Ebrahimi M, Jafari P, Esmaillzadeh A, Asemi Z (2017) Probiotic supplementation in diabetic hemodialysis patients has beneficial metabolic effects. Kidney Int 91:435–442. https://doi.org/10.1016/j.kint.2016.09.040

    Article  CAS  PubMed  Google Scholar 

  28. Adlbrecht C, Hoetzenecker K, Posch M, Steiner S, Kopp C, Hacker S, Auer J, Horvath R, Moser B, Roth G, Wolner E, Lang IM, Ankersmit HJ (2007) Elevated levels of interleukin-1β-converting enzyme and caspase-cleaved cytokeratin-18 in acute myocardial infarction. Eur J Clin Investig 37:372–380. https://doi.org/10.1111/j.1365-2362.2007.01803.x

    Article  CAS  Google Scholar 

  29. Roth GA, Krenn C, Brunner M, Moser B, Ploder M, Spittler A, Pelinka L, Sautner T, Wolner E, Boltz-Nitulescu G, Ankersmit HJ (2004) Elevated serum levels of epithelial cell apoptosis-specific cytokeratin 18 neoepitope M30 in critically ill patients. Shock 22:218–220. https://doi.org/10.1097/01.shk.0000136098.49672.0e

    Article  CAS  PubMed  Google Scholar 

  30. Bantel H, Ruck P, Gregor M, Schulze-Osthoff K (2001) Detection of elevated caspase activation and early apoptosis in liver diseases. Eur J Cell Biol 80:230–239. https://doi.org/10.1078/0171-9335-00154

    Article  CAS  PubMed  Google Scholar 

  31. Kramer G, Erdal H, Mertens HJMM, Nap M, Mauermann J, Steiner G, Marberger M, Bivén K, Shoshan MC, Linder S (2004) Differentiation between cell death modes using measurements of different soluble forms of extracellular cytokeratin 18. Cancer Res 64:1751–1756. https://doi.org/10.1158/0008-5472.CAN-03-2455

    Article  CAS  PubMed  Google Scholar 

  32. Suliman ME, Johnson RJ, García-López E, Qureshi AR, Molinaei H, Carrero JJ, Heimbürger O, Bárány P, Axelsson J, Lindholm B, Stenvinkel P (2006) J-shaped mortality relationship for uric acid in CKD. Am J Kidney Dis 48:761–771. https://doi.org/10.1053/j.ajkd.2006.08.019

    Article  CAS  PubMed  Google Scholar 

  33. Martínez-Moreno JM, Herencia C, de Oca AM, Díaz-Tocados JM, Vergara N, Gómez-Luna MJ, López-Argüello SD, Camargo A, Peralbo-Santaella E, Rodríguez-Ortiz ME, Canalejo A, Rodríguez M, Muñoz-Castañeda JR, Almadén Y (2017) High phosphate induces a pro-inflammatory response by vascular smooth muscle cells and modulation by vitamin D derivatives. Clin Sci 131:1449–1463. https://doi.org/10.1042/CS20160807

    Article  CAS  PubMed  Google Scholar 

  34. Kelly G (2008) Inulin-type prebiotics--a review: part 1. Altern Med Rev 13:315–329. https://doi.org/10.1519/SSC.0b013e318281f689

    Article  PubMed  Google Scholar 

  35. Hünkerler Z, Köken T, Koca B, Kahraman A (2017) Role of uremic toxins on apoptosis with varying periods of hemodialysis. Ther Apher Dial 21(1):38–42. https://doi.org/10.1111/1744-9987.12504

    Article  CAS  PubMed  Google Scholar 

  36. Burkart JM, Bargman JM (2009) Adequacy of peritoneal dialysis, including fluid balance. In: Khanna R, Krediet RT (eds) Nolph and Gokal’s textbook of peritoneal dialysis, 3rd edn. Springer, New York, pp 469–503

    Chapter  Google Scholar 

  37. Chapman CMC, Gibson GR, Rowland I (2011) Health benefits of probiotics: are mixtures more effective than single strains? Eur J Nutr 50:1–17

    Article  CAS  Google Scholar 

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Acknowledgments

We thank all the volunteers who participated in this study. We are grateful to Tak Gen Zist (Company, Tehran, Iran) for providing Bioflora® (a multispecies probiotic supplement) for the present study. The authors would like to thank the staff of the Emam Khomeini dialysis center (Ahvaz, Iran) for their assistance with this project.

Funding

This study was supported by grants from Vice Chancellor of Research, Ahvaz University of Medical Sciences (Ahvaz, Iran).

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Authors and Affiliations

  1. Department of Nutrition, Nutrition and Metabolic Diseases Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Neda Haghighat & Majid Mohammadshahi

  2. Department of Nutrition, Hyperlipidemia Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Majid Mohammadshahi

  3. Department of Nephrology, Golestan Hospital, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Shokouh Shayanpour

  4. Department of Biostatistics and Epidemiology, Faculty of Public Health, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Mohammad Hossein Haghighizadeh

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  1. Neda Haghighat
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Correspondence to Majid Mohammadshahi.

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Haghighat, N., Mohammadshahi, M., Shayanpour, S. et al. Effect of Synbiotic and Probiotic Supplementation on Serum Levels of Endothelial Cell Adhesion Molecules in Hemodialysis Patients: a Randomized Control Study. Probiotics & Antimicro. Prot. 11, 1210–1218 (2019). https://doi.org/10.1007/s12602-018-9477-9

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