Yoghurt with encapsulated probiotic microorganisms for the type 2 diabetes mellitus prevention

Among the main factors resulting from the onset and development of type 2 diabetes mellitus (T2DM), the state of human intestinal microbiota is a leading factor. Studies of the effect of probiotic preparations and products on the condition of T2DM patients and the main markers of the disease, caused both on animals and humans, confirmed their antidiabetic properties — reducing fasting blood glucose levels, glycated hemoglobin, some inflammatory markers, improving the antioxidant effect. Also, the results of studies confirm the possibility of preventing the impact of the disease on the intestinal microflora. Pro- and prebiotics are used to correct the composition of the microbiota.

The research objectives are to develop a multi-strain probiotic functional food ingredient in an encapsulated form, to study the stability of probiotic microorganisms in the composition of a fermented milk product and its effect on its properties.

The microorganism strains with confirmed probiotic effect were used: Bifidobacterium bifidum BF3 DSM 29040; Lactobacillus plantarum 8P A3; Lacticaseibacillus rhamnosus GG. The encapsulated form of probiotics was applied by extrusion method on encapsulator B-390 (BUCHI, Switzerland) using sodium alginate and suspension of probiotic microorganisms with cell concentration not less than 10¹⁰ CFU/g. The resulting capsules had an average diameter of 715 ± 80 μm and an encapsulation efficiency of more than 90%. Addition of encapsulated probiotics to yogurt without filler and with filler in the dry form of functional complex mixture does not significantly affect the physicochemical and structural-mechanical parameters of the product. When considering organoleptic indicators in yogurt without filler, a slight peculiarity is noted in yogurt without filler, which is absent in sandy product with filler. During refrigeration storage for 29 days the concentration of viable encapsulated probiotic microorganisms remained at the level of 10⁹ CFU/g.

1. Mozaffarian D. Dietary and Policy Priorities for Cardiovascular Disease, Diabetes, and Obesity: A Comprehensive Review. Circulation. 2016; 133(2): 187–225. https://doi.org/10.1161/CIRCULATIONAHA.115.018585

2. Oleskin A.V., Shenderov B.A. Probiotics, psychobiotics and metabiotics: problems and prospects. Physical and rehabilitation medicine, medical rehabilitation. 2020; 2(3): 233–243 (in Russian). https://doi.org/10.36425/rehab25811

3. Kiprushkina E.I. et al. The importance of nutrition in the forming of intestinal microbiome. Journal International Academy of Refrigeration. 2020; (2): 52–59 (in Russian). https://doi.org/10.17586/1606-4313-2020-19-2-52-59

4. Malesza I.J. et al. High-Fat, Western-Style Diet, Systemic Inflammation, and Gut Microbiota: A Narrative Review. Cells. 2021; 10(11): 3164. https://doi.org/10.3390/cells10113164

5. Erion K.A., Corkey B.E. Hyperinsulinemia: a Cause of Obesity?. Current Obesity Reports. 2017; 6(2): 178–186. https://doi.org/10.1007/s13679-017-0261-z

6. Drapkina O.M., Korneeva O.N. Gut microbiota and obesity: Pathogenetic relationships and ways to normalize the intestinal microflora. Therapeutic archive. 2016; 88(9): 135–142 (in Russian). https://doi.org/10.17116/terarkh2016889135-142

7. Adeshirlarijaney A., Gewirtz A.T. Considering gut microbiota in treatment of type 2 diabetes mellitus. Gut Microbes. 2020; 11(3): 253–264. https://doi.org/10.1080/19490976.2020.1717719

8. Razmpoosh E., Javadi M., Ejtahed H.-S., Mirmiran P. Probiotics as beneficial agents in the management of diabetes mellitus: a systematic review. Diabetes/Metabolism Research and Reviews. 2016; 32(2): 143–168. https://doi.org/10.1002/dmrr.2665

9. Pokhilenko V.D., Dunaytsev I.A., Kalmantaev T.A., Levchuk V.P., Somov A.N., Chukina I.A. Development of a method for symbiotic bacteria encapsulation. Bacteriology. 2023; 8(3): 16–25 (in Russian). https://www.elibrary.ru/btgihk

10. Tabuchi M. et al. Antidiabetic Effect of Lactobacillus GG in Streptozotocin-induced Diabetic Rats. Bioscience, Biotechnology, and Biochemistry. 2003; 67(6): 1421–1424. https://doi.org/10.1271/bbb.67.1421

11. Li X. et al. Effects of Lactobacillus plantarum CCFM0236 on hyperglycaemia and insulin resistance in high‐fat and streptozotocin‐induced type 2 diabetic mice. Journal of Applied Microbiology. 2016; 121(6): 1727–1736. https://doi.org/10.1111/jam.13276

12. Honda K., Moto M., Uchida N., He F., Hashizume N. Antidiabetic effects of lactic acid bacteria in normal and type 2 diabetic mice. Journal of Clinical Biochemistry and Nutrition. 2012; 51(2): 96–101. https://doi.org/10.3164/jcbn.11-07

13. Chen P. et al. Antidiabetic effect of Lactobacillus casei CCFM0412 on mice with type 2 diabetes induced by a high-fat diet and streptozotocin. Nutrition. 2014; 30(9): 1061–1068. https://doi.org/10.1016/j.nut.2014.03.022

14. Yun S.I., Park H.O., Kang J.H. Effect of Lactobacillus gasseri BNR17 on blood glucose levels and body weight in a mouse model of type 2 diabetes. Journal of Applied Microbiology. 2009; 107(5): 1681–1686. https://doi.org/10.1111/j.1365-2672.2009.04350.x

15. Andreasen A.S. et al. Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. British Journal of Nutrition. 2010; 104(12): 1831–1838. https://doi.org/10.1017/S0007114510002874

16. Yadav H., Jain S., Sinha P.R. Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats. Journal of Dairy Research. 2008; 75(2): 189–195. https://doi.org/10.1017/S0022029908003129

17. Yadav H., Jain S., Sinha P.R. Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition. 2007; 23(1): 62–68. https://doi.org/10.1016/j.nut.2006.09.002

18. Cani P.D., Joly E., Horsmans Y., Delzenne N.M. Oligofructose promotes satiety in healthy human: a pilot study. European Journal of Clinical Nutrition. 2006; 60(5): 567–572. https://doi.org/10.1038/sj.ejcn.1602350

19. Cani P.D. et al. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. The American Journal of Clinical Nutrition. 2009; 90(5): 1236–1243. https://doi.org/10.3945/ajcn.2009.28095

20. Parnell J.A., Reimer R.A. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. The American Journal of Clinical Nutrition. 2009; 89(6): 1751–1759. https://doi.org/10.3945/ajcn.2009.27465

21. Clarke G., Stilling R.M., Kennedy P.J., Stanton C., Cryan J.F., Dinanl T.G. Minireview: Gut Microbiota: The Neglected Endocrine Organ. Molecular Endocrinology. 2014; 28(8): 1221–1238. https://doi.org/10.1210/me.2014-1108

22. Cani P.D., Knauf C., Iglesias M.A., Drucker D.J., Delzenne N.M., Burcelin R. Improvement of Glucose Tolerance and Hepatic Insulin Sensitivity by Oligofructose Requires a Functional Glucagon-Like Peptide 1 Receptor. Diabetes. 2006; 55(5): 1484–1490. https://doi.org/10.2337/db05-1360

23. Cani P.D. et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009; 58(8): 1091–1103. https://doi.org/10.1136/gut.2008.165886

24. Moliboga E.A., Sukhostav E.V., Kozlova O.A., Zinich A.V. Functional Food Market Analysis: Russian and International Aspects. Food Processing: Techniques and Technology. 2022; 52(4): 775–786 (in Russian). https://doi.org/10.21603/2074-9414-2022-4-2405

25. Dahiya D.K. et al. Gut Microbiota Modulation and Its Relationship with Obesity Using Prebiotic Fibers and Probiotics: A Review. Frontiers in Microbiology. 2017; 8: 563. https://doi.org/10.3389/fmicb.2017.00563

26. Jakubowicz D., Froy O. Biochemical and metabolic mechanisms by which dietary whey protein may combat obesity and Type 2 diabetes. The Journal of Nutritional Biochemistry. 2013; 24(1): 1–5. https://doi.org/10.1016/j.jnutbio.2012.07.008

27. Agarkova E.Yu., Ryazantseva K.A., Kruchinin A.G. Anti-Diabetic Activity of Whey Proteins. Food Processing: Techniques and Technology. 2020; 50(2): 306–318 (in Russian). https://doi.org/10.21603/2074-9414-2020-2-306-318

28. Akhavan T., Luhovyy B.L., Brown P.H., Cho C.E., Anderson G.H. Effect of premeal consumption of whey protein and its hydrolysate on food intake and postmeal glycemia and insulin responses in young adults. The American Journal of Clinical Nutrition. 2010; 91(4): 966–975. https://doi.org/10.3945/ajcn.2009.28406

29. Ziai S.A. et al. Psyllium decreased serum glucose and glycosylated hemoglobin significantly in diabetic outpatients. Journal of Ethnopharmacology. 2005; 102(2): 202–207. https://doi.org/10.1016/j.jep.2005.06.042

30. Tosh S.M. Effects of Oats on Carbohydrate Metabolism. Chu Y. (ed.). Oats Nutrition and Technology. Wiley. 2013; 281–297. https://doi.org/10.1002/9781118354100.ch13

31. Wolever T.M.S. et al. Physicochemical properties of oat β-glucan influence its ability to reduce serum LDL cholesterol in humans: a randomized clinical trial. The American Journal of Clinical Nutrition. 2010; 92(4): 723–732. https://doi.org/10.3945/ajcn.2010.29174

32. Nakamura Y., Yamamoto N., Sakai K., Takano T. Antihypertensive Effect of Sour Milk and Peptides Isolated from It That are Inhibitors to Angiotensin I-Converting Enzyme. Journal of Dairy Science. 1995; 78(6): 1253–1257. https://doi.org/10.3168/jds.S0022-0302(95)76745-5

33. Darmov I.V., Chicherin I.Yu., Pogorelsky I.P., Lundovskikh I.A., Durnev E.A. Survival of probiotic microorganisms in the gastrointestinal tract of experimental animals. Journal Infectology. 2012; 4(1): 68–74 (in Russian). https://www.elibrary.ru/nktcyz

34. Darmov I.V., Chicherin I.Yu., Erdyakova A.S., Pogorelsky I.P., Lundovskikh I.A. Comparative assessment of survival of probiotic microorganisms from commercial preparations under the conditions in vitro. Experimental and Clinical Gastroenterology. 2011; (9): 96–101 (in Russian). https://www.elibrary.ru/tbzesh

35. Chávarri M., Marañón I., Ares R., Ibáñez F.C., Marzo F., Villarán M.d.C. Microencapsulation of a probiotic and prebiotic in alginate-chitosan capsules improves survival in simulated gastro-intestinal conditions. International journal of Food Microbiology. 2010; 142(1–2): 185–189. https://doi.org/10.1016/j.ijfoodmicro.2010.06.022

36. Voblikova T.V. Viability of the culture of Bifidobacterium bifidum immobilized by microencapsulation in dairy drink and the simulated gastrointestinal liquids. Vestnik MSTU. 2019; 22(3): 305–313 (in Russian). https://www.elibrary.ru/eqzpbo

37. Haponava I.I., Shchеtko V.A., Romanova L.V. Study of the survival of lactobacillus fermentum microcapsulated microorganisms under exposure to adverse environmental factors. Microbial biotechnology: fundamental and applied aspects. Minsk: Belorusskaya nauka. 2021; 13: 32–41 (in Russian). https://doi.org/10.47612/2226-3136-2021-13-32-41

38. Astafieva B.V., Babintsev K.A., Kurbonova M.K., Tyutkov N., Baranenko D.A. Thermal stability of a functional probiotic food ingredient based on encapsulated microorganisms Lactobacillus plantarum SP-A3. Journal International Academy of Refrigeration. 2022; (2): 42–47 (in Russian). https://doi.org/10.17586/1606-4313-2022-21-2-42-47

39. Bakry A.M. et al. Microencapsulation of Oils: A Comprehensive Review of Benefits, Techniques, and Applications. Comprehensive Reviews in Food Science and Food Safety. 2016; 15(1): 143–182. https://doi.org/10.1111/1541-4337.12179

40. Misra S., Pandey P., Dalbhagat C.G., Mishra H.N. Emerging Technologies and Coating Materials for Improved Probiotication in Food Products: a Review. Food and Bioprocess Technology. 2022; 15(5): 998–1039. https://doi.org/10.1007/s11947-021-02753-5

41. Zhu Y., Wang Z., Bai L., Deng J., Zhou Q. Biomaterial-based encapsulated probiotics for biomedical applications: Current status and future perspectives. Materials & Design. 2021; 210: 110018. https://doi.org/10.1016/j.matdes.2021.110018

42. Nazzaro F., Orlando P., Fratianni F., Coppola R. Microencapsulation in food science and biotechnology. Current Opinion in Biotechnology. 2012; 23(2): 182–186. https://doi.org/10.1016/j.copbio.2011.10.001

43. Yeung T.W., Üçok E.F., Tiani K.A., McClements D.J., Sela D.A. Microencapsulation in Alginate and Chitosan Microgels to Enhance Viability of Bifidobacterium longum for Oral Delivery. Frontiers in Microbiology. 2016; 7: 494. https://doi.org/10.3389/fmicb.2016.00494

44. Mohammad N.A., Zaidel D.N.A., Muhamad I.I., Hamid M.A., Yaakob H., Jusoh Y.M.M. Biopolymeric encapsulation of probiotics for improved release properties in the gastrointestinal digestion system. IOP Conference Series: Materials Science and Engineering. 2020; 778: 012033. https://doi.org/10.1088/1757-899X/778/1/012033

45. Cook M.T., Tzortzis G., Charalampopoulos D., Khutoryansky V.V. Microencapsulation of probiotics for gastrointestinal delivery. Journal of Controlled Release. 2012; 162(1): 56–67. https://doi.org/10.1016/j.jconrel.2012.06.003

46. Sventitsky E.N., Toropov D.K., Egorova T.S. Preparation of microencapsulated symbiotic complex of probiotics based on Lactobacillus helveticus using alginate and chitosan. Biotechnology. 2020; 36(2): 56–63 (in Russian). https://www.elibrary.ru/njoobs

47. Somov A.N., Pokhilenko V.D., Dunaytsev I.A., Klykova M.V., Chukina I.A. Alginate-encapsulated probiotics: preparation and some properties. Biotechnology. 2022; 38(5): 44–52 (in Russian). https://doi.org/10.56304/S0234275822050131

48. Petukhova E.V., Krynitskayа A.Yu. Prospects of using microencapsulated probiotic cultures in the food industry. Vestnik Kazanskogo tekhnologicheskogo universiteta. 2014; 17(22): 257–260 (in Russian). https://www.elibrary.ru/talngz

49. Araújo N.G., Barbosa I.M., Lima T.L.S., Moreira R.T., Cardarelli H.R. Development and characterization of lactose-free probiotic goat milk beverage with bioactive rich jambo pulp. Journal of Food Science and Technology. 2022; 59(10): 3806–3818. https://doi.org/10.1007/s13197-022-05399-z