Review Article

Post-menopausal Osteoporosis and Probiotics

Author(s): Sangeeta Huidrom*, Mirza Atif Beg and Tariq Masood

Volume 22, Issue 7, 2021

Published on: 27 October, 2020

Page: [816 - 822] Pages: 7

DOI: 10.2174/1389450121666201027124947

Price: $65

Abstract

Postmenopausal osteoporosis (PMO) is characterized by low bone mass and structural deterioration of bone tissue with increased risk of fracture in postmenopausal women. It is due to the deficiency of estrogen production after menopause, which causes the imbalance in the bone remodeling process where resorption/formation skewed more towards resoption, which leads to bone loss. It causes high morbidity and severe health complication among the affected women. The current PMO therapy has many unwanted side effects and even increases the possibility of tumorigenesis. Therefore, an alternative therapy that is safe and effective is required. Probiotics are dietary supplements consisting of beneficial microbes and when administered in an adequate amount, confer a health benefit to the host. Recent scientific evidences suggested the link between the intestinal microbiota and bone health. This review discusses the process of bone remodeling and the role of intestinal microbiota on the bone metabolism of the host. Further, it summarizes the recent studies of probiotic on an animal model of PMO and also in post postmenopausal women.

Keywords: Postmenopausal osteoporosis (PMO, probiotics, bone remodeling, Gut microbiota, bone health, animal mode.

Graphical Abstract
[1]
Gold EB. The timing of the age at which natural menopause occurs. Obstet Gynecol Clin North Am 2011; 38(3): 425-40.
[http://dx.doi.org/10.1016/j.ogc.2011.05.002] [PMID: 21961711]
[2]
Laird E, Molloy AM, McNulty H, et al. Greater yogurt consumption is associated with increased bone mineral density and physical function in older adults. Osteoporos Int 2017; 28(8): 2409-19.
[http://dx.doi.org/10.1007/s00198-017-4049-5] [PMID: 28462469]
[3]
Mitlak BH, Nussbaum SR. Diagnosis and treatment of osteoporosis. Annu Rev Med 1993; 44: 265-77.
[http://dx.doi.org/10.1146/annurev.me.44.020193.001405] [PMID: 8476248]
[4]
Parvaneh K, Jamaluddin R, Karimi G, Erfani R. Effect of probiotics supplementation on bone mineral content and bone mass density. ScientificWorldJournal 2014; 2014595962
[http://dx.doi.org/10.1155/2014/595962] [PMID: 24587733]
[5]
Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 1996; 312(7041): 1254-9.
[http://dx.doi.org/10.1136/bmj.312.7041.1254] [PMID: 8634613]
[6]
Jilka RL, Takahashi K, Munshi M, Williams DC, Roberson PK, Manolagas SC. Loss of estrogen upregulates osteoblastogenesis in the murine bone marrow. Evidence for autonomy from factors released during bone resorption. J Clin Invest 1998; 101(9): 1942-50.
[http://dx.doi.org/10.1172/JCI1039] [PMID: 9576759]
[7]
Li JY, Tawfeek H, Bedi B, et al. Ovariectomy disregulates osteoblast and osteoclast formation through the T-cell receptor CD40 ligand. Proc Natl Acad Sci USA 2011; 108(2): 768-73.
[http://dx.doi.org/10.1073/pnas.1013492108] [PMID: 21187391]
[8]
Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr Rev 2010; 31(3): 266-300.
[http://dx.doi.org/10.1210/er.2009-0024] [PMID: 20051526]
[9]
Pfeilschifter J, Köditz R, Pfohl M, Schatz H. Changes in proinflammatory cytokine activity after menopause. Endocr Rev 2002; 23(1): 90-119.
[http://dx.doi.org/10.1210/edrv.23.1.0456] [PMID: 11844745]
[10]
Bismar H, Diel I, Ziegler R, Pfeilschifter J. Increased cytokine secretion by human bone marrow cells after menopause or discontinuation of estrogen replacement. J Clin Endocrinol Metab 1995; 80(11): 3351-5.
[PMID: 7593450]
[11]
D’Amelio P, Grimaldi A, Di Bella S, et al. Estrogen deficiency increases osteoclastogenesis up-regulating T cells activity: a key mechanism in osteoporosis. Bone 2008; 43(1): 92-100.
[http://dx.doi.org/10.1016/j.bone.2008.02.017] [PMID: 18407820]
[12]
Weitzmann MN, Roggia C, Toraldo G, Weitzmann L, Pacifici R. Increased production of IL-7 uncouples bone formation from bone resorption during estrogen deficiency. J Clin Invest 2002; 110(11): 1643-50.
[http://dx.doi.org/10.1172/JCI0215687] [PMID: 12464669]
[13]
Eghbali-Fatourechi G, Khosla S, Sanyal A, Boyle WJ, Lacey DL, Riggs BL. Role of RANK ligand in mediating increased bone resorption in early postmenopausal women. J Clin Invest 2003; 111(8): 1221-30.
[http://dx.doi.org/10.1172/JCI200317215] [PMID: 12697741]
[14]
Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 2006; 17(12): 1726-33.
[http://dx.doi.org/10.1007/s00198-006-0172-4] [PMID: 16983459]
[15]
Richman S, Edusa V, Fadiel A, Naftolin F. Low-dose estrogen therapy for prevention of osteoporosis: working our way back to monotherapy. Menopause 2006; 13(1): 148-55.
[http://dx.doi.org/10.1097/01.gme.0000191205.20738.01] [PMID: 16607111]
[16]
Ettinger B, Black DM, Mitlak BH, et al. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. JAMA 1999; 282(7): 637-45.
[http://dx.doi.org/10.1001/jama.282.7.637] [PMID: 10517716]
[17]
Cummings SR, Tice JA, Bauer S, et al. Prevention of breast cancer in postmenopausal women: approaches to estimating and reducing risk. J Natl Cancer Inst 2009; 101(6): 384-98.
[http://dx.doi.org/10.1093/jnci/djp018] [PMID: 19276457]
[18]
Kennel KA, Drake MT. Adverse effects of bisphosphonates: implications for osteoporosis management. Mayo Clin Proc 2009; 84(7): 632-7.
[http://dx.doi.org/10.1016/S0025-6196(11)60752-0] [PMID: 19567717]
[19]
Reid IR. Efficacy, effectiveness and side effects of medications used to prevent fractures. J Intern Med 2015; 277(6): 690-706.
[20]
Rossouw JE, Anderson GL, Prentice RL, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women’s Health Initiative randomized controlled trial. JAMA 2002; 288(3): 321-33.
[http://dx.doi.org/10.1001/jama.288.3.321] [PMID: 12117397]
[21]
Yousf H, Tomar GB, Srivastava RK. Probiotics and bone health: it takes GUTS to improve bone density. Int J Immunother Cancer Res 2015; 1: 5.
[22]
Britton RA, Irwin R, Quach D, et al. Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 2014; 229(11): 1822-30.
[http://dx.doi.org/10.1002/jcp.24636] [PMID: 24677054]
[23]
Li JY, Chassaing B, Tyagi AM, et al. Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest 2016; 126(6): 2049-63.
[http://dx.doi.org/10.1172/JCI86062] [PMID: 27111232]
[24]
Dar HY, Pal S, Shukla P, et al. Bacillus clausii inhibits bone loss by skewing Treg-Th17 cell equilibrium in postmenopausal osteoporotic mice model. Nutrition 2018; 54: 118-28.
[http://dx.doi.org/10.1016/j.nut.2018.02.013] [PMID: 29793054]
[25]
Takayanagi H. Osteoimmunology and the effects of the immune system on bone. Nat Rev Rheumatol 2009; 5(12): 667-76.
[http://dx.doi.org/10.1038/nrrheum.2009.217] [PMID: 19884898]
[26]
Taichman RS. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 2005; 105(7): 2631-9.
[http://dx.doi.org/10.1182/blood-2004-06-2480] [PMID: 15585658]
[27]
Eriksen EF, Axelrod DW, Melsen F. Bone Histomorphometry. New York: Raven Press 1994; pp. 1-12.
[28]
Courpron P, Meunier P, Vignon G. [Dynamics of bone remodeling explained by Harold Frost. Theory of the B. M.U. (basic multicellular unit)]. Nouv Presse Med 1975; 4(6): 421-4.
[PMID: 1129095]
[29]
Roodman GD. Cell biology of the osteoclast. Exp Hematol 1999; 27(8): 1229-41.
[http://dx.doi.org/10.1016/S0301-472X(99)00061-2] [PMID: 10428500]
[30]
Chambers TJ, Fuller K. Bone cells predispose bone surfaces to resorption by exposure of mineral to osteoclastic contact. J Cell Sci 1985; 76: 155-65.
[PMID: 4066784]
[31]
Crockett JC, Rogers MJ, Coxon FP, Hocking LJ, Helfrich MH. Bone remodelling at a glance. J Cell Sci 2011; 124(Pt 7): 991-8.
[http://dx.doi.org/10.1242/jcs.063032] [PMID: 21402872]
[32]
Everts V, Delaissé JM, Korper W, et al. The bone lining cell: its role in cleaning Howship’s lacunae and initiating bone formation. J Bone Miner Res 2002; 17(1): 77-90.
[http://dx.doi.org/10.1359/jbmr.2002.17.1.77] [PMID: 11771672]
[33]
Silver IA, Murrills RJ, Etherington DJ. Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts. Exp Cell Res 1988; 175(2): 266-76.
[http://dx.doi.org/10.1016/0014-4827(88)90191-7] [PMID: 3360056]
[34]
Delaissé JM, Andersen TL, Engsig MT, Henriksen K, Troen T, Blavier L. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc Res Tech 2003; 61(6): 504-13.
[http://dx.doi.org/10.1002/jemt.10374] [PMID: 12879418]
[35]
Xing L, Boyce BF. Regulation of apoptosis in osteoclasts and osteoblastic cells. Biochem Biophys Res Commun 2005; 328(3): 709-20.
[http://dx.doi.org/10.1016/j.bbrc.2004.11.072] [PMID: 15694405]
[36]
Howard GA, Bottemiller BL, Turner RT, Rader JI, Baylink DJ. Parathyroid hormone stimulates bone formation and resorption in organ culture: evidence for a coupling mechanism. Proc Natl Acad Sci USA 1981; 78(5): 3204-8.
[http://dx.doi.org/10.1073/pnas.78.5.3204] [PMID: 6942425]
[37]
Sims NA, Martin TJ. Coupling the activities of bone formation and resorption: a multitude of signals within the basic multicellular unit. Bonekey Rep 2014; 3: 481.
[http://dx.doi.org/10.1038/bonekey.2013.215] [PMID: 24466412]
[38]
Lind M, Deleuran B, Thestrup-Pedersen K, Søballe K, Eriksen EF, Bünger C. Chemotaxis of human osteoblasts. APMIS1995 103(2): 140-6.
[http://dx.doi.org/10.1111/j.1699-0463.1995.tb01089.x]
[39]
Kini U, Nandeesh BN. Physiology of bone formation, remodelling, and metabolism.Radionuclide and hybrid bone imaging. Berlin, Heidelberg: Springer 2012; pp. 29-57.
[http://dx.doi.org/10.1007/978-3-642-02400-9_2]
[40]
Sjögren K, Engdahl C, Henning P, et al. The gut microbiota regulates bone mass in mice. J Bone Miner Res 2012; 27(6): 1357-67.
[http://dx.doi.org/10.1002/jbmr.1588] [PMID: 22407806]
[41]
Novince CM, Whittow CR, Aartun JD, et al. Commensal Gut Microbiota Immunomodulatory Actions in Bone Marrow and Liver have Catabolic Effects on Skeletal Homeostasis in Health. Sci Rep 2017; 7(1): 5747.
[http://dx.doi.org/10.1038/s41598-017-06126-x] [PMID: 28720797]
[42]
Blanton LV, Charbonneau MR, Salih T, et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 2016; 351(6275)aad3311
[http://dx.doi.org/10.1126/science.aad3311] [PMID: 26912898]
[43]
Yan J, Herzog JW, Tsang K, et al. Gut microbiota induce IGF-1 and promote bone formation and growth. Proc Natl Acad Sci USA 2016; 113(47): E7554-63.
[http://dx.doi.org/10.1073/pnas.1607235113] [PMID: 27821775]
[44]
Guss JD, Horsfield MW, Fontenele FF, et al. Alterations to the gut microbiome impair bone strength and tissue material properties. J Bone Miner Res 2017; 32(6): 1343-53.
[http://dx.doi.org/10.1002/jbmr.3114] [PMID: 28244143]
[45]
Collins KH, Paul HA, Reimer RA, Seerattan RA, Hart DA, Herzog W. Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: studies in a rat model. Osteoarthritis Cartilage 2015; 23(11): 1989-98.
[http://dx.doi.org/10.1016/j.joca.2015.03.014] [PMID: 26521745]
[46]
Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science 2005; 307(5717): 1915-20.
[http://dx.doi.org/10.1126/science.1104816] [PMID: 15790844]
[47]
Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science 2006; 312(5778): 1355-9.
[http://dx.doi.org/10.1126/science.1124234] [PMID: 16741115]
[48]
Moore WEC, Holdeman LV. Discussion of current bacteriologic investigations of the relationships between intestinal flora, diet, and colon cancer. Cancer Res 1975; 35: 3418-20.
[49]
Savage DC. Interactions between the host and its microbes.Microbial ecology of the gut New York. Academic 1977; pp. 277-310.
[50]
Takayanagi H. New immune connections in osteoclast formation. Ann N Y Acad Sci 2010; 1192: 117-23.
[http://dx.doi.org/10.1111/j.1749-6632.2009.05303.x] [PMID: 20392226]
[51]
Kruger MC, Fear A, Chua W-H, Plimmer GG, Schollum LM. The effect of Lactobacillus rhamnosus HN001 on mineral absorption and bone health in growing male and ovariectomised female rats. Dairy Sci Technol 2009; 2009(89): 219-31.
[http://dx.doi.org/10.1051/dst/2009012]
[52]
Rodrigues FC, Castro ASB, Rodrigues VC, et al. Yacon flour and Bifidobacterium longum modulate bone health in rats. J Med Food 2012; 15(7): 664-70.
[http://dx.doi.org/10.1089/jmf.2011.0296] [PMID: 22510044]
[53]
Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP Gastroenterology 2007; 132(6): 2131-57.
[54]
Yadav VK, Ryu JH, Suda N, et al. Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 2008; 135(5): 825-37.
[http://dx.doi.org/10.1016/j.cell.2008.09.059] [PMID: 19041748]
[55]
Zhang J, Motyl KJ, Irwin R, MacDougald OA, Britton RA, McCabe LR. Loss of bone and Wnt10b expression in male type 1 diabetic mice is blocked by the probiotic L. reuteri. Endocrinology 2015; 156(9): 3169-82.
[http://dx.doi.org/10.1210/EN.2015-1308] [PMID: 26135835]
[56]
Chiang SS, Pan TMJ. 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 2011; 59(14): 7734-42.
[http://dx.doi.org/10.1021/jf2013716] [PMID: 21668014]
[57]
Ohlsson C, Engdahl C, Fåk F, et al. Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS One 2014; 9(3)e92368
[http://dx.doi.org/10.1371/journal.pone.0092368] [PMID: 24637895]
[58]
Parvaneh K, Ebrahimi M, Sabran MR, et al. 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; 2015897639
[http://dx.doi.org/10.1155/2015/897639] [PMID: 26366421]
[59]
Kim JG, Lee E, Kim SH, Whang KY, Oh S, Imm JY. Effects of a Lactobacillus casei 393 fermented milk product on bone metabolism in ovariectomised rats. Int Dairy J 2009; 19: 690-5.
[http://dx.doi.org/10.1016/j.idairyj.2009.06.009]
[60]
Dar HY, Shukla P, Mishra PK, et al. Lactobacillus acidophilus inhibits bone loss and increases bone heterogeneity in osteoporotic mice via modulating Treg-Th17 cell balance. Bone Rep 2018; 8: 46-56.
[http://dx.doi.org/10.1016/j.bonr.2018.02.001] [PMID: 29955622]
[61]
Narva M, Rissanen J, Halleen J, Vapaatalo H, Väänänen K, Korpela R. Effects of bioactive peptide, valyl-prolyl-proline (VPP), and lactobacillus helveticus fermented milk containing VPP on bone loss in ovariectomized rats. Ann Nutr Metab 2007; 51(1): 65-74.
[http://dx.doi.org/10.1159/000100823] [PMID: 17356257]
[62]
Kim DE, Kim JK, Han SK, Jang SE, Han MJ, Kim DH. Lactobacillus plantarum NK3 and Bifidobacterium longum NK49 Alleviate Bacterial Vaginosis and Osteoporosis in Mice by Suppressing NF-κB-Linked TNF-α Expression. J Med Food 2019; 22(10): 1022-31.
[http://dx.doi.org/10.1089/jmf.2019.4419] [PMID: 31381476]
[63]
Parvaneh M, Karimi G, Jamaluddin R, Ng MH, Zuriati I, Muhammad SI. Lactobacillus helveticus (ATCC 27558) upregulates Runx2 and Bmp2 and modulates bone mineral density in ovariectomy-induced bone loss rats. Clin Interv Aging 2018; 13: 1555-64.
[http://dx.doi.org/10.2147/CIA.S169223] [PMID: 30214175]
[64]
Jafarnejad S, Djafarian K, Fazeli MR, Yekaninejad MS, Rostamian A, Keshavarz SA. Effects of a multispecies probiotic supplement on bone health in osteopenic postmenopausal women: a randomized, double-blind, controlled trial. J Am Coll Nutr 2017; 36(7): 497-506.
[http://dx.doi.org/10.1080/07315724.2017.1318724] [PMID: 28628374]
[65]
Narva M, Nevala R, Poussa T, Korpela R. The effect of Lactobacillus helveticus fermented milk on acute changes in calcium metabolism in postmenopausal women. Eur J Nutr 2004; 43(2): 61-8.
[http://dx.doi.org/10.1007/s00394-004-0441-y] [PMID: 15083312]
[66]
Jansson PA, Curiac D, Ahrén IL, Hansson F, Niskanen TM, Sjögren K. 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. Lancet Rheumatology 2019; 1: 154-62.
[http://dx.doi.org/10.1016/S2665-9913(19)30068-2]
[67]
Nilsson AG, Sundh D, Bäckhed F, Lorentzon M. Lactobacillus reuteri reduces bone loss in older women with low bone mineral density: a randomized, placebo-controlled, double-blind, clinical trial. J Intern Med 2018; 284(3): 307-17.
[http://dx.doi.org/10.1111/joim.12805] [PMID: 29926979]
[68]
Takimoto T, Hatanaka M, Hoshino T, et al. Effect of Bacillus subtilis C-3102 on bone mineral density in healthy postmenopausal Japanese women: a randomized, placebo-controlled, double-blind clinical trial. Biosci Microb Food H 2018; 37(4): 87-96.
[http://dx.doi.org/10.12938/bmfh.18-006] [PMID: 30370192]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy