Abstract
Bone fragility, despite relatively high BMD values, is an important complication related to insulin resistance and oxidative stress in diabetes mellitus type 1. The present study aimed to compare the effects of soy milk (SM), soy milk containing Lactobacillus casei (PSM), and soy milk enriched with Lactobacillus casei and omega-3 (OPSM) on the stereology of the tibia and vertebra, and antioxidant activity in type 1 diabetic rats. Sixty-five male Sprague Dawley rats were randomly assigned into 5 groups of 13 animals each. Diabetes was induced by a single injection of STZ (60 mg/kg); two control groups (non-diabetic: CN and diabetic: CD) were selected and then fed with 1 mL of distilled water. Three treatment groups were fed 1 ml of SM, PSM, and OPSM via intragastric gavage for 60 days. Treatment with SM, PSM, and OPSM significantly decreased (P < 0.05) the number of the osteoclasts in both tibia and L5 vertebra, and plasma alkaline phosphatase level. Also, the osteoblast number, calcium level, catalase activity, and total antioxidant capacity were increased in the SM, PSM, and OPSM groups compared to the STZ group. OPSM had the greatest effects on the stereological and biochemical parameters compared to the SM and PSM groups. Soy milk combination with Lactobacillus casei and omega-3 can ameliorate the stereological changes in the tibia and vertebra. In addition, this combination increased the antioxidant activity and improved the redox homeostasis in diabetic rats. These results suggest the potential role of soy milk containing Lactobacillus casei enriched with omega-3 in preventing and delaying osteoporosis in diabetic patients.
Similar content being viewed by others
References
Koenig RJ, Peterson CM, Jones RL, Saudek C, Lehrman M, Cerami A (1976) Correlation of glucose regulation and hemoglobin AIc in diabetes mellitus. N Engl J Med 295(8):417–420. https://doi.org/10.1056/NEJM197608192950804
Tarlton JF, Wilkins LJ, Toscano MJ, Avery NC, Knott L (2013) Reduced bone breakage and increased bone strength in free range laying hens fed omega-3 polyunsaturated fatty acid supplemented diets. Bone 52(2):578–586. https://doi.org/10.1016/j.bone.2012.11.003
Gale EA (2002) The rise of childhood type 1 diabetes in the 20th century. Diabetes 51(12):3353–3361
Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporos Int 18(4):427–444. https://doi.org/10.1007/s00198-006-0253-4
Saller A, Maggi S, Romanato G, Tonin P, Crepaldi G (2008) Diabetes and osteoporosis. Aging Clin Exp Res 20(4):280–289. https://doi.org/10.2337/diaclin.20.3.153
Fitzpatrick LA (2002) Secondary causes of osteoporosis. In: Mayo Clinic Proceedings, vol 5. Elsevier, p 453–468
Al-Hariri M (2016) Sweet bones: the pathogenesis of bone alteration in diabetes. J Diabetes Res 2016:1–5. https://doi.org/10.1155/2016/6969040
Safaei H, Janghorbani M, Aminorroaya A, Amini M (2007) Lovastatin effects on bone mineral density in postmenopausal women with type 2 diabetes mellitus. Acta Diabetol 44(2):76–82. https://doi.org/10.1007/s00592-007-0246-6
Pawlowski JW, Martin BR, McCabe GP, McCabe L, Jackson GS, Peacock M, Barnes S, Weaver CM (2015) Impact of equol-producing capacity and soy-isoflavone profiles of supplements on bone calcium retention in postmenopausal women: a randomized crossover trial. Am J Clin Nutr 102(3):695–703. https://doi.org/10.3945/ajcn.114.093906
Hakkak R, Shaaf S, Jo CH, Macleod S, Korourian S (2011) Effects of high-isoflavone soy diet vs. casein protein diet and obesity on DMBA-induced mammary tumor development. Oncol Lett 2(1):29–36. https://doi.org/10.3892/ol.2010.202
Kapila S, Sinha P (2006) Antioxidative and hypocholesterolemic effect of Lactobacillus casei ssp casei (biodefensive properties of lactobacilli). Indian J Med Sci 60(9):361–370
Gilliland SE (1990) Health and nutritional benefits from lactic acid bacteria. FEMS Microbiol Rev 7(1–2):175–188. https://doi.org/10.1016/0378-1097(90)90705-U
Kano M, Takayanagi T, Harada K, Sawada S, Ishikawa F (2006) Bioavailability of isoflavones after ingestion of soy beverages in healthy adults. J Nutr 136(9):2291–2296. https://doi.org/10.1093/jn/136.9.2291
Montazeri-Najafabady N, Ghasemi Y, Dabbaghmanesh MH, Talezadeh P, Koohpeyma F, Gholami A (2018) Supportive role of probiotic strains in protecting rats from ovariectomy-induced cortical bone loss. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-018-9443-6
Schepper JD, Irwin R, Kang J, Dagenais K, Lemon T, Shinouskis A, Parameswaran N, McCabe LR (2017) Probiotics in gut-bone signaling. Adv Exp Med Biol 1033:225–247. https://doi.org/10.1007/978-3-319-66653-2_11
Alokail MS, Sabico S, Al-Saleh Y, Al-Daghri NM, Alkharfy KM, Vanhoutte PM, McTernan PG (2013) Effects of probiotics in patients with diabetes mellitus type 2: study protocol for a randomized, double-blind, placebo-controlled trial. Trials 14(1):195. https://doi.org/10.1186/1745-6215-14-195
Yadav H, Jain S, Sinha P (2007) Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutr 23(1):62–68. https://doi.org/10.1016/j.nut.2006.09.002
Orchard TS, Pan X, Cheek F, Ing SW, Jackson RD (2012) A systematic review of omega-3 fatty acids and osteoporosis. Br J Nutr 107(S2):S253–S260. https://doi.org/10.1017/S0007114512001638
Noorafshan A, Dabbaghmanesh M, Tanideh N, Koohpeyma F, Rasooli R, Hajihoseini M, Bakhshayeshkaram M, Hosseinabadi O (2015) Stereological study of the effect of black olive hydroalcoholic extract on osteoporosis in vertebra and tibia in ovariectomized rats. Osteoporos Int 26(9):2299–2307. https://doi.org/10.1007/s00198-015-3126-x
Dabbaghmanesh MH, Noorafshan A, Talezadeh P, Tanideh N, Koohpeyma F, Iraji A, Bakhshayeshkaram M, Montazeri-Najafabady N (2017) Stereological investigation of the effect of Elaeagnus angustifolia fruit hydroalcoholic extract on osteoporosis in ovariectomized rats. Avicenna J Phytomed 7(3):261–274
Noorafshan A, Hoseini L, Karbalay-Doust S, Nadimi E (2012) A simple stereological method for estimating the number and the volume of the pancreatic beta cells. JOP 13(4):427–432. https://doi.org/10.6092/1590-8577/802
Boyce RW, Dorph-Petersen KA, Lyck L, Gundersen HJ (2010) Design-based stereology: introduction to basic concepts and practical approaches for estimation of cell number. Toxicol Pathol 38(7):1011–1025. https://doi.org/10.1177/0192623310385140
Hofbauer LC, Brueck CC, Singh SK, Dobnig H (2007) Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 22(9):1317–1328. https://doi.org/10.1359/jbmr.070510
Britton RA, Irwin R, Quach D, Schaefer L, Zhang J, Lee T, Parameswaran N, McCabe LR (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229(11):1822–1830. https://doi.org/10.1002/jcp.24636
Blanton C (2018) Bone response to dietary co-enrichment with powdered whole grape and probiotics. Nutrients 10. https://doi.org/10.3390/nu10020146
Zhang J, Motyl KJ, Irwin R, MacDougald OA, Britton RA, McCabe LR (2015) Loss of bone and Wnt10b expression in male type 1 diabetic mice is blocked by the probiotic Lactobacillus reuteri. Endocrinol 156(9):3169–3182. https://doi.org/10.1210/en.2015-1308
Taguchi H, Chen H, Yano R, Shoumura S (2006) Comparative effects of milk and soy milk on bone loss in adult ovariectomized osteoporosis rat. Okajimas Folia Anat 83(2):S; Bawa SE (2010) The significance of soy protein and soy bioactive compounds in the prophylaxis and treatment of osteoporosis. J Osteoporos 2010:1–8. https://doi.org/10.4061/2010/891058
Arjmandi B, Khalil D, Lucas E, Juma S, Sinichi N, Hodges B, Hammond L, Payton M, Munson M, Wild R (2001) Soy protein with its isoflavones improves bone markers in middle-aged and elderly women. In: FASEB J. vol 5. Federation Amer Soc Exp Biol 9650 rockville pike, bethesda, MD 20814-3998 USA, p A728-A728
Punaro GR, Maciel FR, Rodrigues AM, Rogero MM, Bogsan CSB, Oliveira MN, Ihara SSM, Araujo SRR, Sanches TRC, Andrade LC, Higa EMS (2014) Kefir administration reduced progression of renal injury in STZ-diabetic rats by lowering oxidative stress. Nitric Oxide 37:53–60. https://doi.org/10.1016/j.niox.2013.12.012
Sharma P, Bhardwaj P, Singh R (2016) Administration of Lactobacillus casei and Bifidobacterium bifidum ameliorated hyperglycemia, dyslipidemia, and oxidative stress in diabetic rats. Int J Prev Med 7:102. https://doi.org/10.4103/2008-7802.188870
Zhang Q, Wu Y, Fei X (2016) Effect of probiotics on glucose metabolism in patients with type 2 diabetes mellitus: a meta-analysis of randomized controlled trials. Medicina 52(1):28–34
Miraghajani M, Dehsoukhteh SS, Rafie N, Hamedani SG, Sabihi S, Ghiasvand R (2017) Potential mechanisms linking probiotics to diabetes: a narrative review of the literature. Sao Paulo Med J 135(2):169–178
Parvaneh K, Jamaluddin R, Karimi G, Erfani R (2014) Effect of probiotics supplementation on bone mineral content and bone mass density. Sci World J 2014:1–6. https://doi.org/10.1155/2014/595962
McCabe LR, Irwin R, Schaefer L, Britton RA (2013) Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 228(8):1793–1798
Casado-Díaz A, Santiago-Mora R, Dorado G, Quesada-Gómez JM (2012) The omega-6 arachidonic fatty acid, but not the omega-3 fatty acids, inhibits osteoblastogenesis and induces adipogenesis of human mesenchymal stem cells: potential implication in osteoporosis. Osteoporos Int 24(5):1647–1661. https://doi.org/10.1007/s00198-012-2138-z
Nälsén C, Vessby B, Berglund L, Uusitupa M, Hermansen K, Riccardi G, Rivellese A, Storlien L, Erkkilä A, Ylä-Herttuala S, Tapsell L, Basu S (2006) Dietary (n-3) fatty acids reduce the plasma F2-isoprostanes but not prostaglandin F2α in healthy humans. J Nutr 136(5):1222–1228. https://doi.org/10.1093/jn/136.5.1222
Wu WH, Lu SC, Wang TF, Jou HJ, Wang TA (2006) Effects of docosahexaenoic acid supplementation on the blood lipids, estrogen metabolism, and in vivo oxidative stress in postmenopausal vegetarian women. Eur J Clin Nutr 60(3):386–392. https://doi.org/10.1038/sj.ejcn.1602328
Lee Y-B, Lee HJ, Kim KS, Lee J-Y, Nam S-Y, Cheon S-H, Sohn H-S (2004) Evaluation of the preventive effect of isoflavone extract on bone loss in ovariectomized rats. Biosci Biotechnol Biochem 68(5):1040–1045
Morabito N, Crisafulli A, Vergara C, Gaudio A, Lasco A, Frisina N, D’Anna R, Corrado F, Pizzoleo MA, Cincotta M (2002) Effects of genistein and hormone-replacement therapy on bone loss in early postmenopausal women: a randomized double-blind placebo-controlled study. J Bone Miner Res 17(10):1904–1912
Narva M, Nevala R, Poussa T, Korpela R (2004) The effect of Lactobacillus helveticus fermented milk on acute changes in calcium metabolism in postmenopausal women. Eur J Nutr 43(2):61–68
Acknowledgments
The authors wish to thank Dr. Shokrpour at the Research Consultation Center (RCC) of Shiraz University of Medical Sciences for his invaluable assistance in editing this manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All institutional and national guidelines for the care and use of laboratory animals were followed. The study protocols were approved by the Institutional Animal Ethics Committee of Shiraz University of Medical Sciences (Shiraz, Iran) and followed NIH guidelines for care and use of animals (NIH publication No. 85-23, revised in 1996).
Conflict of Interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Bayat, M., Dabbaghmanesh, M.H., Koohpeyma, F. et al. The Effects of Soy Milk Enriched with Lactobacillus casei and Omega-3 on the Tibia and L5 Vertebra in Diabetic Rats: a Stereological Study. Probiotics & Antimicro. Prot. 11, 1172–1181 (2019). https://doi.org/10.1007/s12602-018-9482-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12602-018-9482-z