Skip to main content

Probiotic Soy Milk Consumption and Renal Function Among Type 2 Diabetic Patients with Nephropathy: a Randomized Controlled Clinical Trial

Abstract

Diabetic nephropathy (DN) is one the most important complications of diabetes leading to end-stage renal disease. Dietary approaches have been considered to control of the kidney function deterioration among these patients. The aim of the present study was to determine the effects of fortified soy milk with Lactobacillus plantarum A7 on renal function biomarkers in type 2 DN patients. Forty-eight DN subjects were attended to this parallel randomized trial study. Participants were randomly assigned to consume a diet containing 200 mL/day probiotic soy milk in intervention group or soy milk in the control condition for 8 weeks. An inflammatory adipokine—Progranulin (PGRN), a cytokine receptor-soluble tumor necrosis factor receptor 1 (sTNFR1), and serum levels of Neutrophil gelatinase-associated lipocalin (NGAL) and cystatin C (Cys-C) as the new renal function biomarkers were measured after 8 weeks of intervention according to the standard protocol. Our analysis showed that consumption of probiotic soy milk resulted in a significant reduction in the Cys-C and PGRN levels compared with the soy milk (P = 0.01) in the final adjusted model. In addition, after adjustment for age, weight, and energy intake, a marginally significant in the NGAL level was seen between two groups (P = 0.05). However, there was no significant differences on the sTNFR1concenteration between two groups (P = 0.06). Overall, intake of probiotic soy milk may have a beneficial effect on the renal function in patients with DN.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Eboh C, Chowdhury TA (2015) Management of diabetic renal disease. Ann Transl Med 3:154. https://doi.org/10.3978/j.issn.2305-5839.2015.06.25

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Azimi P, Ghiasvand R, Feizi A, Hosseinzadeh J, Bahreynian M, Hariri M, Khosravi-Boroujeni H (2016) Effect of cinnamon, cardamom, saffron and ginger consumption on blood pressure and a marker of endothelial function in patients with type 2 diabetes mellitus: a randomized controlled clinical trial. Blood Press 3:133–140. https://doi.org/10.3109/08037051.2015.1111020

    CAS  Article  Google Scholar 

  3. Lala MA, Nazar CMJ, Lala HA, Singh JK (2015) Interrelation between blood pressure and diabetes. J Renal Endocrinol 1(1):e05

    Google Scholar 

  4. Amiri M (2016) Diabetes mellitus type 2; an international challenge. Ann Res Dial 1:e04. 

    Google Scholar 

  5. Zhao J, Zhu Y, Hyun N, Zeng D, Uppal K, Tran VT, Yu T, Jones D, He J, Lee ET, Howard BV (2015) Novel metabolic markers for the risk of diabetes development in American Indians. Diabetes Care 38:220–227. https://doi.org/10.2337/dc14-2033

    CAS  Article  PubMed  Google Scholar 

  6. Mahboobi S, Iraj B, Maghsoudi Z, Feizi A, Ghiasvand R, Askari G, Maayeshi N (2014) The effects of probiotic supplementation on markers of blood lipids, and blood pressure in patients with prediabetes: a randomized clinical trial. Int J Prev Med 5:1239–1246

    PubMed  PubMed Central  Google Scholar 

  7. Nasri H (2013) On the occasion of the world diabetes day 2013; diabetes education and prevention; a nephrology point of view. J Renal Inj Prev 2:31

    PubMed  PubMed Central  Google Scholar 

  8. Ardalan M-R, Nasri H (2014) Lessons from our paleolithic primogenitors; a short look to the world diabetes day 2014 with the theme of “healthy living and diabetes”. J Parathyr Dis 2:57–58

    Google Scholar 

  9. Whitham D (2014) Nutrition for the prevention and treatment of chronic kidney disease in diabetes. Can J Diabetes 38:344–348. https://doi.org/10.1016/j.jcjd.2014.07.222

    Article  PubMed  Google Scholar 

  10. Nasri H (2016) From intestine to kidney; a narrative literature review. Acta Persica Pathophysiologica 1:e03

    Google Scholar 

  11. Meek RL, LeBoeuf RC, Saha SA, Alpers CE, Hudkins KL, Cooney SK, Anderberg RJ, Tuttle KR (2013) Glomerular cell death and inflammation with high-protein diet and diabetes. Nephrol Dial Transplant 28:1711–1720. https://doi.org/10.1093/ndt/gfs579

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Miraghajani MS, Esmaillzadeh A, Najafabadi MM, Mirlohi M, Azadbakht L (2012) Soy milk consumption, inflammation, coagulation, and oxidative stress among type 2 diabetic patients with nephropathy. Diabetes Care 35:1981–1985. https://doi.org/10.2337/dc12-0250

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Baharvand-Ahmadi B, Bahmani M, Tajeddini P, Naghdi N, Rafieian-Kopaei M (2016) An ethno-medicinal study of medicinal plants used for the treatment of diabetes. J Nephropathol 5:44

    Article  PubMed  Google Scholar 

  14. Patel R, DuPont HL (2015) New approaches for bacteriotherapy: prebiotics, new-generation probiotics, and synbiotics. Clin Infect Dis 2:S108–S121. https://doi.org/10.1093/cid/civ177

    Article  Google Scholar 

  15. Asemi Z, Zare Z, Shakeri H, Sabihi SS, Esmaillzadeh A (2013) Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Ann Nutr Metab 63:1–9. https://doi.org/10.1159/000349922

    CAS  Article  PubMed  Google Scholar 

  16. Zaman Huri H, Fun Wee H (2013) Drug related problems in type 2 diabetes patients with hypertension: a cross-sectional retrospective study. BMC Endocr Disord 13:2. https://doi.org/10.1186/1472-6823-13-2

    Article  PubMed  PubMed Central  Google Scholar 

  17. Nasri H (2016) A short look to the nephroprotective impacts of metformin. Toxicologia Persa 1:e01

    Google Scholar 

  18. Miraghajani MS, Najafabadi MM, Surkan PJ, Esmaillzadeh A, Mirlohi M, Azadbakht L (2013) Soy milk consumption and blood pressure among type 2 diabetic patients with nephropathy. J Renal Nutr: Off J Council Renal Nutr National Kidney Found 23(277–282):e271. https://doi.org/10.1053/j.jrn.2013.01.017

    CAS  Article  Google Scholar 

  19. Hariri M, Salehi R, Feizi A, Mirlohi M, Ghiasvand R, Habibi N (2015) A randomized, double-blind, placebo-controlled, clinical trial on probiotic soy milk and soy milk: effects on epigenetics and oxidative stress in patients with type II diabetes. Genes Nutr 10:52. https://doi.org/10.1007/s12263-015-0503-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Hojs R, Ekart R, Bevc S, Hojs N (2015) Biomarkers of renal disease and progression in patients with diabetes. J Clin Med 4:1010–1024. https://doi.org/10.3390/jcm4051010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Azadbakht L, Atabak S, Esmaillzadeh A (2008) Soy protein intake, cardiorenal indices, and C-reactive protein in type 2 diabetes with nephropathy: a longitudinal randomized clinical trial. Diabetes Care 31:648–654. https://doi.org/10.2337/dc07-2065

    CAS  Article  PubMed  Google Scholar 

  22. Babashahi M, Mirlohi M, Ghiasvand R, Azadbakht L (2015) Comparison of soymilk and probiotic soymilk effects on serum high-density lipoprotein cholesterol and low-density lipoprotein cholesterol in diabetic Wistar rats. ARYA Atheroscler 11:88–93

    PubMed  PubMed Central  Google Scholar 

  23. Takagi A, Kano M, Kaga C (2015) Possibility of breast cancer prevention: use of soy isoflavones and fermented soy beverage produced using probiotics. Int J Mol Sci 16:10907–10920. https://doi.org/10.3390/ijms160510907

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Yang SO, Kim SH, Cho S, Lee J, Kim YS, Yun SS, Choi HK (2009) Classification of fermented soymilk during fermentation by 1H NMR coupled with principal component analysis and elucidation of free-radical scavenging activities. Biosci Biotechnol Biochem 73:1184–1188. https://doi.org/10.1271/bbb.80743

    CAS  Article  PubMed  Google Scholar 

  25. Fiseha T (2015) Urinary biomarkers for early diabetic nephropathy in type 2 diabetic patients. Biomarker Res 3:16. https://doi.org/10.1186/s40364-015-0042-3

    Article  Google Scholar 

  26. Abbasi B, Ghiasvand R, Mirlohi M (2017) Kidney function improvement by soy milk containing Lactobacillus plantarum A7 in type 2 diabetic patients with nephropathy: a double-blinded randomized controlled trial. Iran J Kidney Dis 11:36–43

    PubMed  Google Scholar 

  27. Wang IK, Wu YY, Yang YF, Ting IW, Lin CC, Yen TH, Chen JH, Wang CH, Huang CC, Lin HC (2015) The effect of probiotics on serum levels of cytokine and endotoxin in peritoneal dialysis patients: a randomised, double-blind, placebo-controlled trial. Benef Microbes 6:423–430. https://doi.org/10.3920/BM2014.0088

    Article  PubMed  Google Scholar 

  28. Liu ZM, Ho SC, Chen YM, Tang N, Woo J (2014) Effect of whole soy and purified isoflavone daidzein on renal function--a 6-month randomized controlled trial in equol-producing postmenopausal women with prehypertension. Clin Biochem 47:1250–1256. https://doi.org/10.1016/j.clinbiochem.2014.05.054

    CAS  Article  PubMed  Google Scholar 

  29. Nicoletto BB, Canani LH (2015) The role of progranulin in diabetes and kidney disease. Diabetol Metab Syndr 7:117. https://doi.org/10.1186/s13098-015-0112-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Gomes AC, Bueno AA, de Souza RG, Mota JF (2014) Gut microbiota, probiotics and diabetes. Nutr J 13:60. https://doi.org/10.1186/1475-2891-13-60

    Article  PubMed  PubMed Central  Google Scholar 

  31. Zarrati M, Salehi E, Nourijelyani K, Mofid V, Zadeh MJ, Najafi F, Ghaflati Z, Bidad K, Chamari M, Karimi M, Shidfar F (2014) Effects of probiotic yogurt on fat distribution and gene expression of proinflammatory factors in peripheral blood mononuclear cells in overweight and obese people with or without weight-loss diet. J Am Coll Nutr 33:417–425. https://doi.org/10.1080/07315724.2013.874937

    Article  PubMed  Google Scholar 

  32. Gohda T, Tomino Y (2013) Novel biomarkers for the progression of diabetic nephropathy: soluble TNF receptors. Curr Diab Rep 13(4):560–566. https://doi.org/10.1007/s11892-013-0385-9

    CAS  Article  PubMed  Google Scholar 

  33. Gohda T, Niewczas MA, Ficociello LH, Walker WH, Skupien J, Rosetti F, Cullere X, Johnson AC, Crabtree G, Smiles AM, Mayadas TN, Warram JH, Krolewski AS (2012) Circulating TNF receptors 1 and 2 predict stage 3 CKD in type 1 diabetes. J Am Soc Nephrol 23:516–524. https://doi.org/10.1681/ASN.2011060628

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Fernandez-Real JM, Lainez B, Vendrell J, Rigla M, Castro A, Penarroja G, Broch M, Perez A, Richart C, Engel P, Ricart W (2002) Shedding of TNF-alpha receptors, blood pressure, and insulin sensitivity in type 2 diabetes mellitus. Am J Physiol Endocrinol Metab 282:E952–E959. https://doi.org/10.1152/ajpendo.00444.2001

    CAS  Article  PubMed  Google Scholar 

  35. Stadlbauer V, Mookerjee RP, Hodges S, Wright GA, Davies NA, Jalan R (2008) Effect of probiotic treatment on deranged neutrophil function and cytokine responses in patients with compensated alcoholic cirrhosis. J Hepatol 48:945–951. https://doi.org/10.1016/j.jhep.2008.02.015

    CAS  Article  PubMed  Google Scholar 

  36. Wu SH, Shu XO, Chow WH, Xiang YB, Zhang X, Li HL, Cai Q, Ji BT, Cai H, Rothman N, Gao YT, Zheng W, Yang G (2012) Soy food intake and circulating levels of inflammatory markers in Chinese women. J Acad Nutr Diet 112:996–1004, 1004 e1001-1004. https://doi.org/10.1016/j.jand.2012.04.001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. See D, Mason S, Roshan R (2002) Increased tumor necrosis factor alpha (TNF-alpha) and natural killer cell (NK) function using an integrative approach in late stage cancers. Immunol Investig 31:137–153

    CAS  Article  Google Scholar 

  38. Miraghajani M, Zaghian N, Mirlohi M, Feizi A, Ghiasvand R (2017) The impact of probiotic soy milk consumption on oxidative stress among type 2 diabetic kidney disease patients: a randomized controlled clinical trial. Journal of Renal Nutrition 27:317-324.

  39. Shahreza FD (2016) From oxidative stress to endothelial cell dysfunction. J Prev Epidemiol 1:e04

    Google Scholar 

  40. Shahreza FD (2016) Mechanistic impact of renal tubular cell protection by antioxidants. Ann Res Antioxid 1:e11

    Google Scholar 

  41. Sabatino A, Regolisti G, Cosola C, Gesualdo L, Fiaccadori E (2017) Intestinal microbiota in type 2 diabetes and chronic kidney disease. Curr Diab Rep 17:16

    Article  PubMed  Google Scholar 

  42. Han JL, Lin HL (2014) Intestinal microbiota and type 2 diabetes: from mechanism insights to therapeutic perspective. World J Gastroentero 20:17737–17745. https://doi.org/10.3748/wjg.v20.i47.17737

    CAS  Article  Google Scholar 

  43. Gomes AC, Bueno AA, de Souza RGM, Mota JF (2014) Gut microbiota, probiotics and diabetes. Nutr J 13. https://doi.org/10.1186/1475-2891-13-60

  44. Nasri H (2016) Aggravating role of inflammation in diabetic kidney disease. J Inj Inflamm 1:e03

    Google Scholar 

  45. Tian P, Li B, He C, Song W, Hou A, Tian S, Meng X, Li K, Shan Y (2016) Antidiabetic (type 2) effects of Lactobacillus G15 and Q14 in rats through regulation of intestinal permeability and microbiota. Food Funct 7:3789–3797

    CAS  Article  PubMed  Google Scholar 

  46. Razmpoosh E, Javadi M, Ejtahed HS, Mirmiran P (2016) Probiotics as beneficial agents in the management of diabetes mellitus: a systematic review. Diabetes Metab Res Rev 32:143–168

    Article  PubMed  Google Scholar 

  47. Rad A, Sahhaf F, Hassanalilou T, Ejtahed H, Motayagheni N, Soroush A, Javadi M, Mortazavian A, Khalili L (2016) Diabetes management by probiotics: current knowledge and future perspectives. Current diabetes reviews https://www.ncbi.nlm.nih.gov/labs/articles/27758705/

Download references

Acknowledgements

The authors appreciate the financial support provided by the Research Council of the Food Security Research Center, Isfahan University of Medical Sciences, Isfahan, Iran.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Reza Ghiasvand.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Miraghajani, M., Zaghian, N., dehkohneh, A. et al. Probiotic Soy Milk Consumption and Renal Function Among Type 2 Diabetic Patients with Nephropathy: a Randomized Controlled Clinical Trial. Probiotics & Antimicro. Prot. 11, 124–132 (2019). https://doi.org/10.1007/s12602-017-9325-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-017-9325-3

Keywords

  • Probiotic soy milk
  • L. plantarum A7
  • Diabetic nephropathy
  • Renal biomarkers