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Published in:

01-04-2018 | Review

Advances in Probiotic Regulation of Bone and Mineral Metabolism

Authors: Laura R. McCabe, Narayanan Parameswaran

Published in: Calcified Tissue International | Issue 4/2018

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.

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–S119

Gogineni V (2013) Probiotics: history and evolution. J Anc Dis Prev Remeidies 1:1–7

Azizpour K et al (2009) History and basic of probiotics. Res J Biol Sci 4:409–426

Ozen M, Dinleyici EC (2015) The history of probiotics: the untold story. Benef Microbes 6(2):159–165PubMedCrossRef

Fontana L et al (2013) Sources, isolation, characterisation and evaluation of probiotics. Br J Nutr 109(Suppl 2):S35–S50PubMedCrossRef

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):68–72PubMedPubMedCentral

Calatayud GA, Suarez JE (2017) A new contribution to the history of probiotics. Benef Microbes 8(2):323–325PubMedCrossRef

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):506–514PubMedCrossRef

McFarland LV (2015) From yaks to yogurt: the history, development, and current use of probiotics. Clin Infect Dis 60(Suppl 2):S85–S90PubMedCrossRef

10.

Gorbach SL (2000) Probiotics and gastrointestinal health. Am J Gastroenterol 95(1 Suppl):S2–S4PubMedCrossRef

11.

Cenci S et al (2000) Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest 106(10):1229–1237PubMedPubMedCentralCrossRef

12.

Hock JM et al (1988) Human parathyroid hormone-(1–34) increases bone mass in ovariectomized and orchidectomized rats. Endocrinology 122(6):2899–2904PubMedCrossRef

13.

Yamada C (2011) [Role of incretins in the regulation of bone metabolism]. Nihon Rinsho 69(5):842–847PubMed

14.

Christakos S et al (2017) Intestinal regulation of calcium: vitamin D and bone physiology. Adv Exp Med Biol 1033:3–12PubMedCrossRef

15.

Ramsey W, Isales CM (2017) Intestinal incretins and the regulation of bone physiology. Adv Exp Med Biol 1033:13–33PubMedCrossRef

16.

Lavoie B, Lian JB, Mawe GM (2017) Regulation of bone metabolism by serotonin. Adv Exp Med Biol 1033:35–46PubMedCrossRef

17.

Ohlsson C et al (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS ONE 9(3):e92368PubMedPubMedCentralCrossRef

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 2015:897639PubMedPubMedCentralCrossRef

19.

Britton RA et al. (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229:1822–1830PubMedPubMedCentralCrossRef

20.

Collins FL et al (2016) Lactobacillus reuteri 6475 increases bone density in intact females only under an inflammatory setting. PLoS ONE 11(4):e0153180PubMedPubMedCentralCrossRef

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):3169–3182PubMedPubMedCentralCrossRef

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):1793–1798PubMedPubMedCentralCrossRef

23.

Sommer F, Bäckhed F (2013) The gut microbiota—masters of host development and physiology. Nat Rev Microbiol 11:227–238PubMedCrossRef

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 351:6275CrossRef

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):854–857PubMedCrossRef

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 55:334–340PubMedCrossRef

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 7:631–637PubMedCrossRef

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:e0144231PubMedPubMedCentralCrossRef

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 106:909–920PubMed

30.

Fukuda S, Ohno H (2014) Gut microbiome and metabolic diseases. Semin Immunopathol 36(1):103–114PubMedCrossRef

31.

Ley RE et al (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444(7122):1022–1023PubMedCrossRef

32.

Derrien M, van Hylckama Vlieg JE (2015) Fate, activity, and impact of ingested bacteria within the human gut microbiota. Trends Microbiol 23(6):354–366PubMedCrossRef

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):5615–5617PubMedPubMedCentralCrossRef

34.

Loh G, Blaut M (2012) Role of commensal gut bacteria in inflammatory bowel diseases. Gut Microbes 3(6):544–555PubMedPubMedCentralCrossRef

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):90–99PubMedCrossRef

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):210–215PubMedCrossRef

37.

Bezkorovainy A (2001) Probiotics: determinants of survival and growth in the gut. Am J Clin Nutr 73(2 Suppl):399S–405SPubMedCrossRef

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)PubMedPubMedCentralCrossRef

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):363–371PubMedPubMedCentralCrossRef

40.

Quach D, Britton RA (2017) Gut microbiota and bone health. Adv Exp Med Biol 1033:47–58PubMedCrossRef

41.

Pacifici R (2017) Bone remodeling and the microbiome. Cold Spring Harb Perspect Med. https://doi.org/10.1101/cshperspect.a031203 PubMed

42.

Blanton LV et al (2016) Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351(6275):aad3311PubMedCrossRef

43.

Schwarzer M et al (2016) Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition. Science 351(6275):854–857PubMedCrossRef

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–E7563PubMedPubMedCentralCrossRef

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):403–414PubMedCrossRef

46.

Hyun S (2013) Body size regulation and insulin-like growth factor signaling. Cell Mol Life Sci 70(13):2351–2365PubMedCrossRef

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):334–340PubMedCrossRef

48.

Sylvester FA (2017) Inflammatory bowel disease: effects on bone and mechanisms. Adv Exp Med Biol 1033:133–150PubMedCrossRef

49.

Whisner CM, Weaver CM (2017) Prebiotics and bone. Adv Exp Med Biol 1033:201–224PubMedCrossRef

50.

Li JY et al (2016) Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest 126(6):2049–2063PubMedPubMedCentralCrossRef

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 e4PubMedCrossRef

52.

Gatej SM et al (2017) Probiotic Lactobacillus rhamnosus GG prevents alveolar bone loss in a mouse model of experimental periodontitis. J Clin Periodontol 45:204–212PubMedCrossRef

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):e0179946PubMedPubMedCentralCrossRef

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):545PubMedPubMedCentralCrossRef

55.

France MM, Turner JR (2017) The mucosal barrier at a glance. J Cell Sci 130(2):307–314PubMedPubMedCentralCrossRef

56.

Konig J et al (2016) Human intestinal barrier function in health and disease. Clin Transl Gastroenterol 7(10):e196PubMedPubMedCentralCrossRef

57.

Nagao-Kitamoto H et al (2016) Pathogenic role of the gut microbiota in gastrointestinal diseases. Intest Res 14(2):127–138PubMedPubMedCentralCrossRef

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

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–R1157PubMedPubMedCentralCrossRef

60.

Irwin R et al (2013) Colitis-induced bone loss is gender dependent and associated with increased inflammation. Inflamm Bowel Dis 19(8):1586–1597PubMedPubMedCentralCrossRef

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–G1029PubMedPubMedCentralCrossRef

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):104–112PubMedCrossRef

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):454–460PubMedCrossRef

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):53–58PubMedCrossRef

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):3317–3328PubMedPubMedCentralCrossRef

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):612–616PubMedCrossRef

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):575–579PubMedCrossRef

68.

Madsen K et al (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121(3):580–591PubMedCrossRef

69.

Zareie M et al (2006) Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut 55(11):1553–1560PubMedPubMedCentralCrossRef

70.

Bron PA et al (2017) Can probiotics modulate human disease by impacting intestinal barrier function? Br J Nutr 117(1):93–107PubMedPubMedCentralCrossRef

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):804–816PubMedCrossRef

72.

Anderson RC et al (2010) Lactobacillus plantarum DSM 2648 is a potential probiotic that enhances intestinal barrier function. FEMS Microbiol Lett 309(2):184–192PubMed

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):731–746PubMedCrossRef

74.

Qin H et al (2009) L. plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol 9:63PubMedPubMedCentralCrossRef

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):350–358PubMedCrossRef

76.

Mowat AM, Agace WW (2014) Regional specialization within the intestinal immune system. Nat Rev Immunol 14(10):667–685PubMedCrossRef

77.

Kundu P et al (2017) Our gut microbiome: the evolving inner self. Cell 171(7):1481–1493PubMedCrossRef

78.

Neurath MF (2014) Cytokines in inflammatory bowel disease. Nat Rev Immunol 14:329–342PubMedCrossRef

79.

Strober W, Fuss IJ (2011) Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases. Gastroenterology 140:1756–1767PubMedPubMedCentralCrossRef

80.

Bjarnason I et al (1997) Reduced bone density in patients with inflammatory bowel disease. Gut 40:228–233PubMedPubMedCentralCrossRef

81.

Zanchetta MB, Longobardi V, Bai JC (2016) Bone and celiac disease. Curr Osteoporos Rep 14:43–48PubMedCrossRef

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):16594–16599PubMedPubMedCentralCrossRef

83.

Ali T et al (2009) Osteoporosis in inflammatory bowel disease. Am J Med 122:599–604PubMedPubMedCentralCrossRef

84.

Ciucci T et al (2015) Bone marrow Th17 TNFα cells induce osteoclast differentiation, and link bone destruction to IBD. Gut 64:1072–1081PubMedCrossRef

85.

Harris L et al (2009) Inflammatory bowel disease causes reversible suppression of osteoblast and chondrocyte function in mice. Am J Physiol 296:G1020–G1029

86.

Irwin R et al (2013) Colitis induced bone loss is gender dependent and associated with increased inflammation. Inflamm Bowel Dis 19:1586PubMedPubMedCentralCrossRef

87.

Metzger CE et al (2017) Inflammatory bowel disease in a rodent model alters osteocyte protein levels controlling bone turnover. J Bone Miner Res 32:802–813PubMedCrossRef

88.

Sjogren K et al (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27:1357–1367PubMedPubMedCentralCrossRef

89.

Li J-Y et al (2016) Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest 126:2049–2063PubMedPubMedCentralCrossRef

90.

Yan J et al (2016) Gut microbiota induce IGF-1 and promote bone formation and growth. Proc Natl Acad Sci USA 113:E7554–E7563PubMedPubMedCentralCrossRef

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.

Klaenhammer TR et al (2012) The impact of probiotics and prebiotics on the immune system. Nat Rev Immunol 12(10):728–734PubMedCrossRef

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):153–158PubMedCrossRef

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 228:1793–1798PubMedPubMedCentralCrossRef

95.

Collins FL et al (2016) Lactobacillus reuteri 6475 increases bone density in intact females only under an inflammatory setting. PLoS ONE 11:e0153180PubMedPubMedCentralCrossRef

96.

Thomas CM et al (2012) Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS ONE 7:e31951PubMedPubMedCentralCrossRef

97.

Ohlsson C et al (2014) Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS ONE 9:e92368PubMedPubMedCentralCrossRef

98.

Wang Z et al (2017) Probiotics protect mice from CoCrMo particles-induced osteolysis. Int J Nanomed 12:5387–5397CrossRef

99.

Salva S et al (2012) Dietary supplementation with probiotics improves hematopoiesis in malnourished mice. PLoS ONE 7(2):e31171PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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

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 59:472–475

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 PubMedCrossRef

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 PubMedCrossRef

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 CrossRef

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 CrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 85:1621–1625PubMed

113.

Plavnik I, Scott ML (1980) Effects of additional vitamins, minerals, or brewer’s yeast upon leg weaknesses in broiler chickens. Poult Sci 59:459–467PubMedCrossRef

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 73:1699–1711PubMedCrossRef

Title: Advances in Probiotic Regulation of Bone and Mineral Metabolism
Authors: Laura R. McCabe
Narayanan Parameswaran
Publication date: 01-04-2018
Publisher: Springer US
Published in: Calcified Tissue International / Issue 4/2018
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI: https://doi.org/10.1007/s00223-018-0403-7

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