Calcified Tissue International

, Volume 102, Issue 4, pp 480–488 | Cite as

Advances in Probiotic Regulation of Bone and Mineral Metabolism

Review

Abstract

Probiotics have been consumed by humans for thousands of years because they are beneficial for long-term storage of foods and promote the health of their host. Ingested probiotics reside in the gastrointestinal tract where they have many effects including modifying the microbiota composition, intestinal barrier function, and the immune system which result in systemic benefits to the host, including bone health. Probiotics benefit bone growth, density, and structure under conditions of dysbiosis, intestinal permeability, and inflammation (recognized mediators of bone loss and osteoporosis). It is likely that multiple mechanisms are involved in mediating probiotic signals from the gut to the bone. Studies indicate a role for the microbiota (composition and activity), intestinal barrier function, and immune cells in the signaling process. These mechanisms are not mutually exclusive, but rather, may synergize to provide benefits to the skeletal system of the host and serve as a starting point for investigation. Given that probiotics hold great promise for supporting bone health and are generally regarded as safe, future studies identifying mechanisms are warranted.

Keywords

Probiotic Microbiota Osteoporosis Lactobacillus Intestine Bone Inflammation Barrier Permeability Colon 

Notes

Acknowledgements

The authors would like to acknowledge funding from the National Institute of Health, Grants RO1 DK101050 and RO1 AT007695.

Conflict of interest

LRM and NP have no conflict of interest.

References

  1. 1.
    Gasbarrini G, Bonvicini F, Gramenzi A (2016) Probiotics history. J Clin Gastroenterol 50 Suppl 2, Proceedings from the 8th Probiotics, Prebiotics & New Foods for Microbiota and Human Health meeting held in Rome, Italy on September 13-15, 2015:S116–S119Google Scholar
  2. 2.
    Gogineni V (2013) Probiotics: history and evolution. J Anc Dis Prev Remeidies 1:1–7Google Scholar
  3. 3.
    Azizpour K et al (2009) History and basic of probiotics. Res J Biol Sci 4:409–426Google Scholar
  4. 4.
    Ozen M, Dinleyici EC (2015) The history of probiotics: the untold story. Benef Microbes 6(2):159–165PubMedCrossRefGoogle Scholar
  5. 5.
    Fontana L et al (2013) Sources, isolation, characterisation and evaluation of probiotics. Br J Nutr 109(Suppl 2):S35–S50PubMedCrossRefGoogle Scholar
  6. 6.
    Anukam KC, Reid G (2007) Organisms associated with bacterial vaginosis in Nigerian women as determined by PCR-DGGE and 16S rRNA gene sequence. Afr Health Sci 7(2):68–72PubMedPubMedCentralGoogle Scholar
  7. 7.
    Calatayud GA, Suarez JE (2017) A new contribution to the history of probiotics. Benef Microbes 8(2):323–325PubMedCrossRefGoogle Scholar
  8. 8.
    Hill C et al (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514PubMedCrossRefGoogle Scholar
  9. 9.
    McFarland LV (2015) From yaks to yogurt: the history, development, and current use of probiotics. Clin Infect Dis 60(Suppl 2):S85–S90PubMedCrossRefGoogle Scholar
  10. 10.
    Gorbach SL (2000) Probiotics and gastrointestinal health. Am J Gastroenterol 95(1 Suppl):S2–S4PubMedCrossRefGoogle Scholar
  11. 11.
    Cenci S et al (2000) Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest 106(10):1229–1237PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Hock JM et al (1988) Human parathyroid hormone-(1–34) increases bone mass in ovariectomized and orchidectomized rats. Endocrinology 122(6):2899–2904PubMedCrossRefGoogle Scholar
  13. 13.
    Yamada C (2011) [Role of incretins in the regulation of bone metabolism]. Nihon Rinsho 69(5):842–847PubMedGoogle Scholar
  14. 14.
    Christakos S et al (2017) Intestinal regulation of calcium: vitamin D and bone physiology. Adv Exp Med Biol 1033:3–12PubMedCrossRefGoogle Scholar
  15. 15.
    Ramsey W, Isales CM (2017) Intestinal incretins and the regulation of bone physiology. Adv Exp Med Biol 1033:13–33PubMedCrossRefGoogle Scholar
  16. 16.
    Lavoie B, Lian JB, Mawe GM (2017) Regulation of bone metabolism by serotonin. Adv Exp Med Biol 1033:35–46PubMedCrossRefGoogle Scholar
  17. 17.
    Ohlsson C et al (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS ONE 9(3):e92368PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Parvaneh K et al. (2015) Probiotics (Bifidobacterium longum) increase bone mass density and upregulate Sparc and Bmp-2 genes in rats with bone loss resulting from ovariectomy. Biomed Res Int 2015:897639PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Britton RA et al. (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229:1822–1830PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Collins FL et al (2016) Lactobacillus reuteri 6475 increases bone density in intact females only under an inflammatory setting. PLoS ONE 11(4):e0153180PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Zhang J et al (2015) Loss of bone and Wnt10b expression in male type 1 diabetic mice is blocked by the probiotic Lactobacillus reuteri. Endocrinology 156(9):3169–3182PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    McCabe LR et al (2013) Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 228(8):1793–1798PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Sommer F, Bäckhed F (2013) The gut microbiota—masters of host development and physiology. Nat Rev Microbiol 11:227–238PubMedCrossRefGoogle Scholar
  24. 24.
    Blanton LV, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, Ilkaveya O, Subramanian S, Manary MJ, Trehan I, Jorgensen JM, Fan Y-M, Henrissat B, Leyn SA, Rodionov DA, Osterman AL, Maleta KM, Newgard CB, Ashorn P, Dewey KG, Gordon JI (2016) Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351:6275CrossRefGoogle Scholar
  25. 25.
    Schwarzer M, Makki K, Storelli G, Machuca-Gayet I, Srutkova D, Hermanova P, Martino ME, Balmand S, Hudcovic T, Heddi A, Rieusset J, Kozakova H, Vidal H, Leulier F (2016) Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351(6275):854–857PubMedCrossRefGoogle Scholar
  26. 26.
    Steenhout PG, Rochat F, Hager C (2009) The effect of Bifidobacterium lactis on the growth of infants: a pooled analysis of randomized controlled studies. Ann Nutr Metab 55:334–340PubMedCrossRefGoogle Scholar
  27. 27.
    Lei M, Hua L-M, Wang D-W (2016) The effect of probiotic treatment on elderly patients with distal radius fracture: a prospective double-blind, placebo-controlled randomised clinical trial. Benef Microbes 7:631–637PubMedCrossRefGoogle Scholar
  28. 28.
    Tu M-Y, Chen H-L, Tung Y-T, Kao C-C, Hu F-C, Chen C-M (2015) Short-term effects of Kefir-fermented milk consumption on bone mineral density and bone metabolism in a randomized clinical trial of osteoporotic patients. PLoS ONE 10:e0144231PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Lambert et al (2017) Combined bioavailable isoflavones and probiotics improve bone status and estrogen metabolism in postmenopausal osteopenic women: a randomized controlled trial. Am J Clin Nutr 106:909–920PubMedGoogle Scholar
  30. 30.
    Fukuda S, Ohno H (2014) Gut microbiome and metabolic diseases. Semin Immunopathol 36(1):103–114PubMedCrossRefGoogle Scholar
  31. 31.
    Ley RE et al (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444(7122):1022–1023PubMedCrossRefGoogle Scholar
  32. 32.
    Derrien M, van Hylckama Vlieg JE (2015) Fate, activity, and impact of ingested bacteria within the human gut microbiota. Trends Microbiol 23(6):354–366PubMedCrossRefGoogle Scholar
  33. 33.
    Oozeer R et al (2006) Survival of Lactobacillus casei in the human digestive tract after consumption of fermented milk. Appl Environ Microbiol 72(8):5615–5617PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Loh G, Blaut M (2012) Role of commensal gut bacteria in inflammatory bowel diseases. Gut Microbes 3(6):544–555PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Firmesse O et al (2008) Lactobacillus rhamnosus R11 consumed in a food supplement survived human digestive transit without modifying microbiota equilibrium as assessed by real-time polymerase chain reaction. J Mol Microbiol Biotechnol 14(1–3):90–99PubMedCrossRefGoogle Scholar
  36. 36.
    Fujimoto J et al (2008) Identification and quantification of Lactobacillus casei strain Shirota in human feces with strain-specific primers derived from randomly amplified polymorphic DNA. Int J Food Microbiol 126(1–2):210–215PubMedCrossRefGoogle Scholar
  37. 37.
    Bezkorovainy A (2001) Probiotics: determinants of survival and growth in the gut. Am J Clin Nutr 73(2 Suppl):399S–405SPubMedCrossRefGoogle Scholar
  38. 38.
    Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72(4):728–764 (Table of Contents)PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    McCabe L, Britton RA, Parameswaran N (2015) Prebiotic and probiotic regulation of bone health: role of the intestine and its microbiome. Curr Osteoporos Rep 13(6):363–371PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Quach D, Britton RA (2017) Gut microbiota and bone health. Adv Exp Med Biol 1033:47–58PubMedCrossRefGoogle Scholar
  41. 41.
    Pacifici R (2017) Bone remodeling and the microbiome. Cold Spring Harb Perspect Med.  https://doi.org/10.1101/cshperspect.a031203 PubMedGoogle Scholar
  42. 42.
    Blanton LV et al (2016) Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351(6275):aad3311PubMedCrossRefGoogle Scholar
  43. 43.
    Schwarzer M et al (2016) Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351(6275):854–857PubMedCrossRefGoogle Scholar
  44. 44.
    Yan J et al (2016) Gut microbiota induce IGF-1 and promote bone formation and growth. Proc Natl Acad Sci USA 113(47):E7554–E7563PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Storelli G et al (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14(3):403–414PubMedCrossRefGoogle Scholar
  46. 46.
    Hyun S (2013) Body size regulation and insulin-like growth factor signaling. Cell Mol Life Sci 70(13):2351–2365PubMedCrossRefGoogle Scholar
  47. 47.
    Steenhout PG, Rochat F, Hager C (2009) The effect of Bifidobacterium lactis on the growth of infants: a pooled analysis of randomized controlled studies. Ann Nutr Metab 55(4):334–340PubMedCrossRefGoogle Scholar
  48. 48.
    Sylvester FA (2017) Inflammatory bowel disease: effects on bone and mechanisms. Adv Exp Med Biol 1033:133–150PubMedCrossRefGoogle Scholar
  49. 49.
    Whisner CM, Weaver CM (2017) Prebiotics and bone. Adv Exp Med Biol 1033:201–224PubMedCrossRefGoogle Scholar
  50. 50.
    Li JY et al (2016) Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest 126(6):2049–2063PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Xiao E et al (2017) Diabetes enhances IL-17 expression and alters the oral microbiome to increase its pathogenicity. Cell Host Microbe 22(1):120–128 e4PubMedCrossRefGoogle Scholar
  52. 52.
    Gatej SM et al (2017) Probiotic Lactobacillus rhamnosus GG prevents alveolar bone loss in a mouse model of experimental periodontitis. J Clin Periodontol 45:204–212PubMedCrossRefGoogle Scholar
  53. 53.
    Ricoldi MST et al (2017) Effects of the probiotic Bifidobacterium animalis subsp. lactis on the non-surgical treatment of periodontitis. A histomorphometric, microtomographic and immunohistochemical study in rats. PLoS ONE 12(6):e0179946PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Kobayashi R et al (2017) Oral administration of Lactobacillus gasseri SBT2055 is effective in preventing Porphyromonas gingivalis-accelerated periodontal disease. Sci Rep 7(1):545PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    France MM, Turner JR (2017) The mucosal barrier at a glance. J Cell Sci 130(2):307–314PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Konig J et al (2016) Human intestinal barrier function in health and disease. Clin Transl Gastroenterol 7(10):e196PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Nagao-Kitamoto H et al (2016) Pathogenic role of the gut microbiota in gastrointestinal diseases. Intest Res 14(2):127–138PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Collins F et al. (2017) Temporal and regional intestinal change in permeability, tight junction and cytokine gene expression following ovariectomy-induced estrogen deficiency. Physiol Rep.  https://doi.org/10.14814/phy2.13263 Google Scholar
  59. 59.
    Irwin R et al (2016) Intestinal inflammation without weight loss decreases bone density and growth. Am J Physiol Regul Integr Comp Physiol 311(6):R1149–R1157PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Irwin R et al (2013) Colitis-induced bone loss is gender dependent and associated with increased inflammation. Inflamm Bowel Dis 19(8):1586–1597PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Harris L et al (2009) Inflammatory bowel disease causes reversible suppression of osteoblast and chondrocyte function in mice. Am J Physiol Gastrointest Liver Physiol 296(5):G1020–G1029PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Tremellen K, Pearce K (2012) Dysbiosis of gut microbiota (DOGMA)—a novel theory for the development of Polycystic Ovarian Syndrome. Med Hypotheses 79(1):104–112PubMedCrossRefGoogle Scholar
  63. 63.
    Maruyama K, Sano G, Matsuo K (2006) Murine osteoblasts respond to LPS and IFN-gamma similarly to macrophages. J Bone Miner Metab 24(6):454–460PubMedCrossRefGoogle Scholar
  64. 64.
    Moriyama H, Ukai T, Hara Y (2002) Interferon-gamma production changes in parallel with bacterial lipopolysaccharide induced bone resorption in mice: an immunohistometrical study. Calcif Tissue Int 71(1):53–58PubMedCrossRefGoogle Scholar
  65. 65.
    Braniste V et al (2009) Oestradiol decreases colonic permeability through oestrogen receptor beta-mediated up-regulation of occludin and junctional adhesion molecule-A in epithelial cells. J Physiol 587(Pt 13):3317–3328PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Rosenfeldt V et al (2004) Effect of probiotics on gastrointestinal symptoms and small intestinal permeability in children with atopic dermatitis. J Pediatr 145(5):612–616PubMedCrossRefGoogle Scholar
  67. 67.
    Stratiki Z et al (2007) The effect of a bifidobacter supplemented bovine milk on intestinal permeability of preterm infants. Early Hum Dev 83(9):575–579PubMedCrossRefGoogle Scholar
  68. 68.
    Madsen K et al (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121(3):580–591PubMedCrossRefGoogle Scholar
  69. 69.
    Zareie M et al (2006) Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut 55(11):1553–1560PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Bron PA et al (2017) Can probiotics modulate human disease by impacting intestinal barrier function? Br J Nutr 117(1):93–107PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Zyrek AA et al (2007) Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol 9(3):804–816PubMedCrossRefGoogle Scholar
  72. 72.
    Anderson RC et al (2010) Lactobacillus plantarum DSM 2648 is a potential probiotic that enhances intestinal barrier function. FEMS Microbiol Lett 309(2):184–192PubMedGoogle Scholar
  73. 73.
    Resta-Lenert S, Barrett KE (2006) Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 130(3):731–746PubMedCrossRefGoogle Scholar
  74. 74.
    Qin H et al (2009) L. plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol 9:63PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Moorthy G, Murali MR, Devaraj SN (2009) Lactobacilli facilitate maintenance of intestinal membrane integrity during Shigella dysenteriae 1 infection in rats. Nutrition 25(3):350–358PubMedCrossRefGoogle Scholar
  76. 76.
    Mowat AM, Agace WW (2014) Regional specialization within the intestinal immune system. Nat Rev Immunol 14(10):667–685PubMedCrossRefGoogle Scholar
  77. 77.
    Kundu P et al (2017) Our gut microbiome: the evolving inner self. Cell 171(7):1481–1493PubMedCrossRefGoogle Scholar
  78. 78.
    Neurath MF (2014) Cytokines in inflammatory bowel disease. Nat Rev Immunol 14:329–342PubMedCrossRefGoogle Scholar
  79. 79.
    Strober W, Fuss IJ (2011) Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases. Gastroenterology 140:1756–1767PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Bjarnason I et al (1997) Reduced bone density in patients with inflammatory bowel disease. Gut 40:228–233PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Zanchetta MB, Longobardi V, Bai JC (2016) Bone and celiac disease. Curr Osteoporos Rep 14:43–48PubMedCrossRefGoogle Scholar
  82. 82.
    Trottier MD et al (2012) Enhanced production of early lineages of monocytic and granulocytic cells in mice with colitis. Proc Natl Acad Sci USA 109(41):16594–16599PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Ali T et al (2009) Osteoporosis in inflammatory bowel disease. Am J Med 122:599–604PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Ciucci T et al (2015) Bone marrow Th17 TNFα cells induce osteoclast differentiation, and link bone destruction to IBD. Gut 64:1072–1081PubMedCrossRefGoogle Scholar
  85. 85.
    Harris L et al (2009) Inflammatory bowel disease causes reversible suppression of osteoblast and chondrocyte function in mice. Am J Physiol 296:G1020–G1029Google Scholar
  86. 86.
    Irwin R et al (2013) Colitis induced bone loss is gender dependent and associated with increased inflammation. Inflamm Bowel Dis 19:1586PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Metzger CE et al (2017) Inflammatory bowel disease in a rodent model alters osteocyte protein levels controlling bone turnover. J Bone Miner Res 32:802–813PubMedCrossRefGoogle Scholar
  88. 88.
    Sjogren K et al (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27:1357–1367PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Li J-Y et al (2016) Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest 126:2049–2063PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Yan J et al (2016) Gut microbiota induce IGF-1 and promote bone formation and growth. Proc Natl Acad Sci USA 113:E7554–E7563PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Quach D et al. (2018) Microbiota reconstitution does not cause bone loss in germ-free mice. mSphere.  https://doi.org/10.1128/mSphereDirect.00545-17
  92. 92.
    Klaenhammer TR et al (2012) The impact of probiotics and prebiotics on the immune system. Nat Rev Immunol 12(10):728–734PubMedCrossRefGoogle Scholar
  93. 93.
    Frei R, Akdis M, O’Mahony L (2015) Prebiotics, probiotics, synbiotics, and the immune system: experimental data and clinical evidence. Curr Opin Gastroenterol 31(2):153–158PubMedCrossRefGoogle Scholar
  94. 94.
    McCabe LR et al (2013) Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol 228:1793–1798PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Collins FL et al (2016) Lactobacillus reuteri 6475 increases bone density in intact females only under an inflammatory setting. PLoS ONE 11:e0153180PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Thomas CM et al (2012) Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS ONE 7:e31951PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Ohlsson C et al (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS ONE 9:e92368PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Wang Z et al (2017) Probiotics protect mice from CoCrMo particles-induced osteolysis. Int J Nanomed 12:5387–5397CrossRefGoogle Scholar
  99. 99.
    Salva S et al (2012) Dietary supplementation with probiotics improves hematopoiesis in malnourished mice. PLoS ONE 7(2):e31171PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Chiang SS, Pan TM (2011) Antiosteoporotic effects of lactobacillus-fermented soy skim milk on bone mineral density and the microstructure of femoral bone in ovariectomized mice. J Agric Food Chem 59:7734–7742.  https://doi.org/10.1021/jf2013716 PubMedCrossRefGoogle Scholar
  101. 101.
    Maekawa T, Hajishengallis G (2014) Topical treatment with probiotic Lactobacillus brevis CD2 inhibits experimental periodontal inflammation and bone loss. J Periodontal Res 49:785–791.  https://doi.org/10.1111/jre.12164 PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Messora MR, Oliveira LFF, Foureaux RC et al (2013) Probiotic therapy reduces periodontal tissue destruction and improves the intestinal morphology in rats with ligature-induced periodontitis. J Periodontol 84:1818–1826.  https://doi.org/10.1902/jop.2013.120644 PubMedCrossRefGoogle Scholar
  103. 103.
    Oliveira LFF, Salvador SL, Silva PHF et al (2016) Benefits of Bifidobacterium animalis subsp. lactis probiotic in experimental periodontitis. J Periodontol.  https://doi.org/10.1902/jop.2016.160217 Google Scholar
  104. 104.
    Ghanem KZ, Badawy IH, ABDEL-SALAM AM (2004) Influence of yoghurt and probiotic yoghurt on the absorption of calcium, magnesium, iron and bone mineralization in rats. Milchwissenschaft 59:472–475Google Scholar
  105. 105.
    Tomofuji T, Ekuni D, Azuma T et al (2012) Supplementation of broccoli or Bifidobacterium longum-fermented broccoli suppresses serum lipid peroxidation and osteoclast differentiation on alveolar bone surface in rats fed a high-cholesterol diet. Nutr Res 32:301–307.  https://doi.org/10.1016/j.nutres.2012.03.006 PubMedCrossRefGoogle Scholar
  106. 106.
    Rodrigues FC, Castro ASB, Rodrigues VC et al (2012) Yacon flour and Bifidobacterium longum modulate bone health in rats. J Med Food 15:664–670.  https://doi.org/10.1089/jmf.2011.0296 PubMedCrossRefGoogle Scholar
  107. 107.
    Kruger MC, Fear A, Chua W-H et al (2009) The effect of Lactobacillus rhamnosus HN001 on mineral absorption and bone health in growing male and ovariectomised female rats. Dairy Sci Technol 89:219–231.  https://doi.org/10.1051/dst/2009012 CrossRefGoogle Scholar
  108. 108.
    Kim JG, Lee E, Kim SH et al (2009) Effects of a Lactobacillus casei 393 fermented milk product on bone metabolism in ovariectomised rats. Int Dairy J 19:690–695.  https://doi.org/10.1016/j.idairyj.2009.06.009 CrossRefGoogle Scholar
  109. 109.
    Narva M, Collin M, Lamberg-Allardt C et al (2004) Effects of long-term intervention with Lactobacillus helveticus-fermented milk on bone mineral density and bone mineral content in growing rats. Ann Nutr Metab 48:228–234.  https://doi.org/10.1159/000080455 PubMedCrossRefGoogle Scholar
  110. 110.
    Amdekar S, Kumar A, Sharma P et al (2012) Lactobacillus protected bone damage and maintained the antioxidant status of liver and kidney homogenates in female wistar rats. Mol Cell Biochem 368:155–165.  https://doi.org/10.1007/s11010-012-1354-3 PubMedCrossRefGoogle Scholar
  111. 111.
    Rovenský J, Švík K, Maťha V et al (2004) The effects of Enterococcus faecium and selenium on methotrexate treatment in rat adjuvant-induced arthritis. Clin Dev Immunol 11:267–273.  https://doi.org/10.1080/17402520400001660 PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Mutuş R, Kocabagli N, Alp M et al (2006) The effect of dietary probiotic supplementation on tibial bone characteristics and strength in broilers. Poult Sci 85:1621–1625PubMedGoogle Scholar
  113. 113.
    Plavnik I, Scott ML (1980) Effects of additional vitamins, minerals, or brewer’s yeast upon leg weaknesses in broiler chickens. Poult Sci 59:459–467PubMedCrossRefGoogle Scholar
  114. 114.
    Nahashon SN, Nakaue HS, Mirosh LW (1994) Production variables and nutrient retention in single comb White Leghorn laying pullets fed diets supplemented with direct-fed microbials. Poult Sci 73:1699–1711PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PhysiologyMichigan State UniversityEast LansingUSA
  2. 2.Department of RadiologyMichigan State UniversityEast LansingUSA
  3. 3.Biomedical Imaging Research CenterMichigan State UniversityEast LansingUSA

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