663
Views
1
CrossRef citations to date
0
Altmetric
Review Articles

Effects of probiotics on bone mineral density and bone turnover: A systematic review

ORCID Icon, , &

References

  • Abbasi, J. 2019. Are probiotics money down the toilet? Or worse? JAMA 321 (7):633–5. doi: 10.1001/jama.2018.20798.
  • Bailey, R. L., K. W. Dodd, J. A. Goldman, J. J. Gahche, J. T. Dwyer, A. J. Moshfegh, C. T. Sempos, and M. F. Picciano. 2010. Estimation of total usual calcium and vitamin D intakes in the United States. The Journal of Nutrition 140 (4):817–22. doi: 10.3945/jn.109.118539.
  • Bezkorovainy, A. 2001. Probiotics: Determinants of survival and growth in the gut. The American Journal of Clinical Nutrition 73 (2 Suppl.):399S–405S. doi: 10.1093/ajcn/73.2.399s.
  • Bliziotes, M., A. Eshleman, B. Burt-Pichat, X. W. Zhang, J. Hashimoto, K. Wiren, and C. Chenu. 2006. Serotonin transporter and receptor expression in osteocytic MLO-Y4 cells. Bone 39 (6):1313–21. doi: 10.1016/j.bone.2006.06.009.
  • Bolland, M. J., A. Grey, and A. Avenell. 2018. Effects of vitamin D supplementation on musculoskeletal health: A systematic review, meta-analysis, and trial sequential analysis. The Lancet. Diabetes & Endocrinology 6 (11):847–58. doi: 10.1016/S2213-8587(18)30265-1.
  • Britton, R. A., R. Irwin, D. Quach, L. Schaefer, J. Zhang, T. Lee, N. Parameswaran, and L. R. McCabe. 2014. Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. Journal of Cellular Physiology 229 (11):1822–30. doi: 10.1002/jcp.24636.
  • Burge, R., B. Dawson-Hughes, D. H. Solomon, J. B. Wong, A. King, and A. Tosteson. 2007. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. Journal of Bone and Mineral Research : The Official Journal of the American Society for Bone and Mineral Research 22 (3):465–75. doi: 10.1359/jbmr.061113.
  • Calatayud, G. A., and J. E. Suarez. 2017. A new contribution to the history of probiotics. Beneficial Microbes 8 (2):323–5. doi: 10.3920/BM2017.x002.
  • Cani, P. D., J. Amar, M. A. Iglesias, M. Poggi, C. Knauf, D. Bastelica, A. M. Neyrinck, F. Fava, K. M. Tuohy, C. Chabo, et al. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56 (7):1761–72. doi: 10.2337/db06-1491.
  • Chen, Y. C., J. Greenbaum, H. Shen, and H. W. Deng. 2017. Association between gut microbiota and bone health: Potential mechanisms and prospective. The Journal of Clinical Endocrinology and Metabolism 102 (10):3635–46. doi: 10.1210/jc.2017-00513.
  • Chiang, S. S., and T. M. Pan. 2013. Beneficial effects of phytoestrogens and their metabolites produced by intestinal microflora on bone health. Applied Microbiology and Biotechnology 97 (4):1489–500. doi: 10.1007/s00253-012-4675-y.
  • Chinese Clinical Trial Register. 2018. Clinical study for probiotics on osteoporosis. ChiCTR 1800019268. [Internet]. http://wwwwhoint/trialsearch/Trial2aspx?TrialID=ChiCTR1800019268
  • Clarke, T. C., L. I. Black, B. J. Stussman, P. M. Barnes, and R. L. Nahin. 2015. Trends in the use of complementary health approaches among adults: United States, 2002-2012. National Health Statistics Reports 1–16 (79)
  • Clinical Trials Registry India. 2018. In this study Bacillus coagulans, a probiotic will be tested for its effectiveness as an additional ­supplement along with regular medicine for osteoporosis. CTRI/2018/02/011756. [Internet]. http://www.who.int/trialsearch/Trial2.aspx?TrialID=CTRI/2018/02/011756
  • ClinicalTrials.gov. 2017. Effect of VSL#3 on Bone Mineral Density in Postmenopausal Women. NCT03165747. [Internet]. https://clinicaltrialsgov/show/NCT03165747
  • ClinicalTrials.gov. 2019a. Prevention of early postmenopausal bone loss with Lactobacillus reuteri – A randomized, placebo-controlled, single centre Clinical Trial. NCT04169789. [Internet]. https://clinicaltrials.gov/ct2/show/NCT04169789
  • ClinicalTrials.gov. 2019b. The effects of a novel probiotic supplement on menopausal symptoms and bone health. NCT04001088. [Internet]. https://clinicaltrialsgov/show/NCT04001088
  • Collins, F. L., R. Irwin, H. Bierhalter, J. Schepper, R. A. Britton, N. Parameswaran, and L. R. McCabe. 2016. Lactobacillus reuteri 6475 increases bone density in intact females only under an inflammatory setting. PLoS One 11 (4):e0153180. doi: 10.1371/journal.pone.0153180.
  • Derrien, M., and J. E. van Hylckama Vlieg. 2015. Fate, activity, and impact of ingested bacteria within the human gut microbiota. Trends in Microbiology 23 (6):354–66. doi: 10.1016/j.tim.2015.03.002.
  • DeSelm, C. J., Y. Takahata, J. Warren, J. C. Chappel, T. Khan, X. Li, C. Liu, Y. Choi, Y. F. Kim, W. Zou, et al. 2012. IL-17 mediates estrogen-deficient osteoporosis in an Act1-dependent manner. Journal of Cellular Biochemistry 113 (9):2895–902. doi: 10.1002/jcb.24165.
  • Eastell, R., and P. Szulc. 2017. Use of bone turnover markers in postmenopausal osteoporosis. The Lancet. Diabetes & Endocrinology 5 (11):908–23. doi: 10.1016/S2213-8587(17)30184-5.
  • Fatoye, F., P. Smith, T. Gebrye, and G. Yeowell. 2019. Real-world persistence and adherence with oral bisphosphonates for osteoporosis: A systematic review. BMJ Open 9 (4):e027049. doi: 10.1136/bmjopen-2018-027049.
  • Foureaux Rde, C., M. R. Messora, L. F. F. de Oliveira, M. H. Napimoga, A. N. J. Pereira, M. S. Ferreira, and L. J. Pereira. 2014. Effects of probiotic therapy on metabolic and inflammatory parameters of rats with ligature-induced periodontitis associated with restraint stress. Journal of Periodontology 85 (7):975–83. doi: 10.1902/jop.2013.130356.
  • Garcia, V. G., L. R. Knoll, M. Longo, V. C. Novaes, N. Z. Assem, E. Ervolino, B. E. de Toledo, and L. H. Theodoro. 2016. Effect of the probiotic Saccharomyces cerevisiae on ligature-induced periodontitis in rats. Journal of Periodontal Research 51 (1):26–37. doi: 10.1111/jre.12274.
  • Gasbarrini, G., F. Bonvicini, and A. Gramenzi. 2016. Probiotics History. Journal of Clinical Gastroenterology 50 (Suppl. 2):S116–S19. doi: 10.1097/MCG.0000000000000697.
  • Goldenberg, J. Z., C. Yap, L. Lytvyn, C. K. Lo, J. Beardsley, D. Mertz, and B. C. Johnston. 2017. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. The Cochrane Database of Systematic Reviews 12:CD006095. doi: 10.1002/14651858.CD006095.pub4.
  • Grossman, D. C., S. J. Curry, D. K. Owens, M. J. Barry, A. B. Caughey, K. W. Davidson, C. A. Doubeni, J. W. Epling, A. R. Kemper, A. H. Krist, et al. 2018. Vitamin D, calcium, or combined supplementation for the primary prevention of fractures in community-dwelling adults: US Preventive Services Task Force Recommendation Statement. JAMA 319 (15):1592–9. doi: 10.1001/jama.2018.3185.
  • Guarner, F., A. G. Khan, J. Garisch, R. Eliakim, A. Gangl, A. Thomson, J. Krabshuis, T. Lemair, P. Kaufmann, J. A. de Paula, et al. 2012. World gastroenterology organisation global guidelines: Probiotics and prebiotics October 2011. Journal of Clinical Gastroenterology 46 (6):468–81. doi: 10.1097/MCG.0b013e3182549092.
  • Guyatt, G., A. D. Oxman, E. A. Akl, R. Kunz, G. Vist, J. Brozek, S. Norris, Y. Falck-Ytter, P. Glasziou, H. DeBeer, et al. 2011. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. Journal of Clinical Epidemiology 64 (4):383–94. doi: 10.1016/j.jclinepi.2010.04.026.
  • Higgins, J. P. T., J. Thomas, J. Chandler, M. Cumpston, T. Li, M. J. Page, et al. 2021. Cochrane Handbook for Systematic Reviews of Interventions version 6.2. Cochrane Collaboration. www.training.cochrane.org/handbook.
  • Hopkins, R. B., N. Burke, C. Von Keyserlingk, W. D. Leslie, S. N. Morin, J. D. Adachi, A. Papaioannou, L. Bessette, J. P. Brown, L. Pericleous, et al. 2016. The current economic burden of illness of osteoporosis in Canada. Osteoporosis International: A Journal Established as Result of Cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 27 (10):3023–32. doi: 10.1007/s00198-016-3631-6.
  • Hou, G. Q., C. Guo, G. H. Song, N. Fang, W. J. Fan, X. D. Chen, L. Yuan, and Z. Q. Wang. 2013. Lipopolysaccharide (LPS) promotes osteoclast differentiation and activation by enhancing the MAPK pathway and COX-2 expression in RAW264.7 cells. International Journal of Molecular Medicine 32 (2):503–10. doi: 10.3892/ijmm.2013.1406.
  • Humphrey, M. B., and M. C. Nakamura. 2016. A comprehensive review of immunoreceptor regulation of osteoclasts. Clinical Reviews in Allergy & Immunology 51 (1):48–58. doi: 10.1007/s12016-015-8521-8.
  • Jackson, R. D., A. Z. LaCroix, M. Gass, R. B. Wallace, J. Robbins, C. E. Lewis, T. Bassford, S. A. Beresford, H. R. Black, P. Blanchette, et al. 2006. Calcium plus vitamin D supplementation and the risk of fractures. New England Journal of Medicine 354 (7):669–83. doi: 10.1056/NEJMoa055218.
  • Jafarnejad, S., K. Djafarian, M. R. Fazeli, M. S. Yekaninejad, A. Rostamian, and S. A. Keshavarz. 2017. Effects of a multispecies probiotic supplement on bone health in osteopenic postmenopausal women: A randomized, double-blind, controlled trial. Journal of the American College of Nutrition 36 (7):497–506. doi: 10.1080/07315724.2017.1318724.
  • Jansson, P.-A., D. Curiac, I. Lazou Ahrén, F. Hansson, N. T. Martinsson, K. Sjögren, and C. Ohlsson. 2019. Probiotic treatment using a mix of three Lactobacillus strains for lumbar spine bone loss in postmenopausal women: A randomised, double-blind, placebo-controlled, multicentre trial. The Lancet Rheumatology 1 (3):e154–e62. doi: 10.1016/S2665-9913(19)30068-2.
  • Johnell, O., and J. A. Kanis. 2006. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporosis International : A Journal Established as Result of Cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 17 (12):1726–33. doi: 10.1007/s00198-006-0172-4.
  • Johnston, C. C., Jr., S. L. Hui, R. M. Witt, R. Appledorn, R. S. Baker, and C. Longcope. 1985. Early menopausal changes in bone mass and sex steroids. The Journal of Clinical Endocrinology and Metabolism 61 (5):905–11. doi: 10.1210/jcem-61-5-905.
  • Kennedy, P. J., J. F. Cryan, T. G. Dinan, and G. Clarke. 2017. Kynurenine pathway metabolism and the microbiota-gut-brain axis. Neuropharmacology 112 (Pt B):399–412. doi: 10.1016/j.neuropharm.2016.07.002.
  • Kitaura, H., K. Kimura, M. Ishida, H. Kohara, M. Yoshimatsu, and T. Takano-Yamamoto. 2013. Immunological reaction in TNF-α-mediated osteoclast formation and bone resorption in vitro and in vivo. Clinical & Developmental Immunology 2013:181849. doi: 10.1155/2013/181849.
  • Lambert, M. N. T., C. B. Thybo, S. Lykkeboe, L. M. Rasmussen, X. Frette, L. P. Christensen, and P. B. Jeppesen. 2017. Combined bioavailable isoflavones and probiotics improve bone status and estrogen metabolism in postmenopausal osteopenic women: A randomized controlled trial. The American Journal of Clinical Nutrition 106 (3):909–20.
  • Li, C., Q. Huang, R. Yang, Y. Dai, Y. Zeng, L. Tao, X. Li, J. Zeng, and Q. Wang. 2019. Gut microbiota composition and bone mineral loss-epidemiologic evidence from individuals in Wuhan, China. Osteoporosis International 30 (5):1003–13. doi: 10.1007/s00198-019-04855-5.
  • Li, J. Y., B. Chassaing, A. M. Tyagi, C. Vaccaro, T. Luo, J. Adams, T. M. Darby, M. N. Weitzmann, J. G. Mulle, A. T. Gewirtz, et al. 2016. Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. Journal of Clinical Investigation 126 (6):2049–63. doi: 10.1172/JCI86062.
  • Lily, S. 2014. The role of isoflavones in menopausal bone loss. Climacteric 17:S29
  • Lindsay, B. R., T. Olufade, J. Bauer, J. Babrowicz, and R. Hahn. 2016. Patient-reported barriers to osteoporosis therapy. Archives of Osteoporosis 11:19. doi: 10.1007/s11657-016-0272-5.
  • McCabe, L. R., and N. Parameswaran. 2018. Advances in probiotic regulation of bone and mineral metabolism. Calcified Tissue International 102 (4):480–8. doi: 10.1007/s00223-018-0403-7.
  • McCabe, L. R., R. Irwin, L. Schaefer, and R. A. Britton. 2013. Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. Journal of Cellular Physiology 228 (8):1793–8. doi: 10.1002/jcp.24340.
  • McFarland, L. V. 2015. From yaks to yogurt: The history, development, and current use of probiotics. Clinical Infectious Diseases 60 (Suppl. 2):S85–S90. doi: 10.1093/cid/civ054.
  • Modi, A., E. S. Siris, J. Tang, and S. Sen. 2015. Cost and consequences of noncompliance with osteoporosis treatment among women initiating therapy. Current Medical Research and Opinion 31 (4):757–65. doi: 10.1185/03007995.2015.1016605.
  • Morato-Martinez, M., B. Lopez-Plaza, C. Santurino, S. Palma-Milla, and C. Gomez-Candela. 2020. A dairy product to reconstitute enriched with bioactive nutrients stops bone loss in high-risk menopausal women without pharmacological treatment. Nutrients 12 (8).2203. doi: 10.3390/nu1208:.
  • Nilsson, A. G., D. Sundh, F. Backhed, and M. Lorentzon. 2018. Lactobacillus reuteri reduces bone loss in older women with low bone mineral density: A randomized, placebo-controlled, double-blind, clinical trial. Journal of Internal Medicine 284 (3):307–17. doi: 10.1111/joim.12805.
  • Ohlsson, C., C. Engdahl, F. Fak, A. Andersson, S. H. Windahl, H. H. Farman, S. Moverare-Skrtic, U. Islander, and K. Sjogren. 2014. Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One 9 (3):e92368. doi: 10.1371/journal.pone.0092368.
  • Ong, A. M., K. Kang, H. A. Weiler, and S. N. Morin. 2020. Fermented milk products and bone health in postmenopausal women: A systematic review of randomized controlled trials, prospective cohorts, and case-control studies. Advances in Nutrition 11 (2):251–65.
  • Page, M. J., J. E. McKenzie, P. M. Bossuyt, I. Boutron, T. C. Hoffmann, C. D. Mulrow, L. Shamseer, J. M. Tetzlaff, E. A. Akl, S. E. Brennan, et al. 2021. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ (Clinical Research ed.) 372:n71. doi: 10.1136/bmj.n71.
  • Parker, E. A., T. Roy, C. R. D’Adamo, and L. S. Wieland. 2018. Probiotics and gastrointestinal conditions: An overview of evidence from the Cochrane Collaboration. Nutrition (Burbank, Los Angeles County, Calif.) 45:125–34.e11. doi: 10.1016/j.nut.2017.06.024.
  • Parvaneh, K., M. Ebrahimi, M. R. Sabran, G. Karimi, A. N. Hwei, S. Abdul-Majeed, Z. Ahmad, Z. Ibrahim, and R. Jamaluddin. 2015. Probiotics (Bifidobacterium longum) increase bone mass density and upregulate sparc and Bmp-2 genes in rats with bone loss resulting from ovariectomy. Biomed Research International 2015:1–10. doi: 10.1155/2015/897639.
  • Ray, N. F., J. K. Chan, M. Thamer, and L. J. Melton. 3rd. 1997. Medical expenditures for the treatment of osteoporotic fractures in the United States in 1995: Report from the National Osteoporosis Foundation. Journal of Bone and Mineral Research : The Official Journal of the American Society for Bone and Mineral Research 12 (1):24–35. doi: 10.1359/jbmr.1997.12.1.24.
  • Rizzoli, R., and E. Biver. 2020. Are probiotics the new calcium and vitamin d for bone health? Current Osteoporosis Reports 18 (3):273–84. doi: 10.1007/s11914-020-00591-6.
  • Rodrigues, F. C., A. S. Castro, V. C. Rodrigues, S. A. Fernandes, E. A. Fontes, T. T. de Oliveira, H. S. Martino, and C. L. de Luces Fortes Ferreira. 2012. Yacon flour and Bifidobacterium longum modulate bone health in rats. Journal of Medicinal Food 15 (7):664–70. doi: 10.1089/jmf.2011.0296.
  • Sambrook, P., and C. Cooper. 2006. Osteoporosis. Lancet (London, England) 367 (9527):2010–8. doi: 10.1016/S0140-6736(06)68891-0.
  • Schepper, J. D., F. Collins, N. D. Rios-Arce, H. J. Kang, L. Schaefer, J. D. Gardinier, R. Raghuvanshi, R. A. Quinn, R. Britton, N. Parameswaran, et al. 2020. Involvement of the gut microbiota and barrier function in glucocorticoid-induced osteoporosis. Journal of Bone and Mineral Research : The Official Journal of the American Society for Bone and Mineral Research 35 (4):801–20. doi: 10.1002/jbmr.3947.
  • Schepper, J. D., F. L. Collins, N. D. Rios-Arce, S. Raehtz, L. Schaefer, J. D. Gardinier, R. A. Britton, N. Parameswaran, and L. R. McCabe. 2019. Probiotic Lactobacillus reuteri prevents postantibiotic bone loss by reducing intestinal dysbiosis and preventing barrier disruption. Journal of Bone and Mineral Research 34 (4):681–98. doi: 10.1002/jbmr.3635.
  • Siris, E. S., S. T. Harris, C. J. Rosen, C. E. Barr, J. N. Arvesen, T. A. Abbott, and S. Silverman. 2006. Adherence to bisphosphonate therapy and fracture rates in osteoporotic women: Relationship to vertebral and nonvertebral fractures from 2 US claims databases. Mayo Clinic Proceedings 81 (8):1013–22. doi: 10.4065/81.8.1013.
  • Sjogren, K., C. Engdahl, P. Henning, U. H. Lerner, V. Tremaroli, M. K. Lagerquist, F. Backhed, and C. Ohlsson. 2012. The gut microbiota regulates bone mass in mice. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research 27 (6):1357–67. doi: 10.1002/jbmr.1588.
  • Sterne, J. A. C., J. Savovic, M. J. Page, R. G. Elbers, N. S. Blencowe, I. Boutron, C. J. Cates, H. Y. Cheng, M. S. Corbett, S. M. Eldridge, et al. 2019. RoB 2: A revised tool for assessing risk of bias in randomised trials. BMJ (Clinical Research ed.) 366:l4898. doi: 10.1136/bmj.l4898.
  • Stoecker, W. V., A. Carson, V. H. Nguyen, A. B. Willis, J. G. Cole, and R. K. Rader. 2017. Addressing the crisis in the treatment of osteoporosis: Better paths forward. Journal of Bone and Mineral Research : The Official Journal of the American Society for Bone and Mineral Research 32 (6):1386–7. doi: 10.1002/jbmr.3145.
  • Su, G. L., C. W. Ko, P. Bercik, Y. Falck-Ytter, S. Sultan, A. V. Weizman, and R. L. Morgan. 2020. AGA clinical practice guidelines on the role of probiotics in the management of gastrointestinal disorders. Gastroenterology 159 (2):697–705. doi: 10.1053/j.gastro.2020.05.059.
  • Tai, V., W. Leung, A. Grey, I. R. Reid, and M. J. Bolland. 2015. Calcium intake and bone mineral density: Systematic review and meta-analysis. BMJ 351:h4183. doi: 10.1136/bmj.h4183.
  • Takimoto, T., M. Hatanaka, T. Hoshino, T. Takara, K. Tanaka, A. Shimizu, H. Morita, and T. Nakamura. 2018. Effect of Bacillus subtilis C-3102 on bone mineral density in healthy postmenopausal Japanese women: A randomized, placebo-controlled, double-blind clinical trial. Bioscience of Microbiota, Food and Health 37 (4):87–96. doi: 10.12938/bmfh.18-006.
  • Zhang, J., K. J. Motyl, R. Irwin, O. A. MacDougald, R. A. Britton, and L. R. McCabe. 2015. Loss of bone and Wnt10b expression in male type 1 diabetic mice is blocked by the probiotic Lactobacillus reuteri. Endocrinology 156 (9):3169–82. doi: 10.1210/EN.2015-1308.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.