AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Food Science and Human Wellness Article
PDF (1.2 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Review Article | Open Access

Targeting gut microbiota in osteoporosis: impact of the microbial based functional food ingredients

Pauline Duffuler, Khushwant S. Bhullar, Jianping Wu( )
Department of Agricultural Food & Nutritional Science, University of Alberta, Edmonton T6G 2P5, Canada

Peer review under responsibility of Tsinghua University Press.

Show Author Information

Abstract

Osteoporosis is the most common bone disorder, characterized by low bone mineral density and microarchitectural deterioration of the bone tissue, which increases the susceptibility to fracture. In the past decade, emerging research findings reported the implication of gut microbiota on bone health and osteoporosis pathology. Osteoporotic patients or individuals with a lower bone mineral density exhibit an alteration of the gut microbiota at several taxonomic levels. Additional reports demonstrate that gut microbiota regulates bone metabolism through the modulation of the gut function (mineral availability and absorption, gut integrity), the immune system, and the endocrine system. Thus, based on the vital role of gut microbiota on bone health, it has emerged as a novel therapeutic target for the prevention of bone loss and the treatment of osteoporosis. Microbial-based functional food ingredients, such as probiotics, prebiotics, synbiotics, and fermented foods, have been developed to alter the gut microbiota composition and function and thus, to provide benefits to the host bone health. Despite promising initial results, microbial-based therapies are still under investigation. Moreover, additional animal studies and clinical trials are needed to understand the interactions between gut microbiota and bone metabolism before further applications.

Keywords

DysbiosisBone healthProbioticPrebioticFermented foodSynbiotic

References

[1]
International Osteoporosis Foundation, Introduction to bone biology: all about our bones, (2022). https://iofbonehealth.org/introduction-bonebiology-all-about-our-bones (accessed April 26, 2020).
[2]

D.J. Hadjidakis, I.I. Androulakis, Bone remodeling, Ann. N Y Acad Sci. 1092 (2006) 385-396. https://doi.org/10.1196/ANNALS.1365.035.
Crossref Google Scholar
[3]

T. Yatsunenko, F.E. Rey, M.J. Manary, et al., Human gut microbiome viewed across age and geography, Nature 486 (2012) 222-227. https://doi.org/10.1038/nature11053.
Crossref Google Scholar
[4]

S.I. Harada, G.A. Rodan, Control of osteoblast function and regulation of bone mass, Nature 423 (2003) 349-355. https://doi.org/10.1038/nature01660.
Crossref Google Scholar
[5]

World Health Organization, Who Scientific Group on the Assessment of Osteoporosis at Primary Health, World Health. May (2007) 1-13. https://doi.org/10.1016/S0140-6736(02)08761-5.
Crossref Google Scholar
[6]
Osteoporosis Canada, About the Disease | Osteoporosis Canada, (n.d.). https://osteoporosis.ca/about-the-disease/ (accessed October 21, 2019).
[7]

N.C. Wright, A.C. Looker, K.G. Saag, et al., The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine, J. Bone Miner. Res. 29 (2014) 2520-2526. https://doi.org/10.1002/jbmr.2269.
Crossref Google Scholar
[8]

J.A. Kanis, N. Norton, N.C. Harvey, et al., SCOPE 2021: a new scorecard for osteoporosis in Europe, Arch Osteoporos. 16 (2021). https://doi.org/10.1007/s11657-020-00871-9.
Crossref Google Scholar
[9]
Government of Canada, Osteoporosis -Canada.ca, (2018). https://www.canada.ca/en/public-health/services/chronic-diseases/osteoporosis.htm (accessed November 3, 2019).
[10]

O. Ström, F. Borgström, J.A. Kanis, et al., Osteoporosis: burden, health care provision and opportunities in the EU, Arch Osteoporos. 6 (2011) 59-155. https://doi.org/10.1007/s11657-011-0060-1.
Crossref Google Scholar
[11]

F. Hawkins, V. Garla, G. Allo, et al., Senile and postmenopausal osteoporosis: pathophysiology, diagnosis, and treatment, Elsevier Inc., 2021. https://doi.org/10.1016/b978-0-12-819667-0.00005-6.
Crossref Google Scholar
[12]

N.B. Watts, J.P. Bilezikian, S.M. Petak, American Association of Clinical Endocrinologists medical guidelines for clinical practice for the diagnosis and treatment of postmenopausal osteoporosis: executive summary of recommendations, Physiol Behav. 176 (2016) 100-106.
Google Scholar
[13]

F. Bäckhed, C.M. Fraser, Y. Ringel, et al., Defining a healthy human gut microbiome: Current concepts, future directions, and clinical applications, Cell Host Microbe. 12 (2012) 611-622. https://doi.org/10.1016/j.chom.2012.10.012.
Crossref Google Scholar
[14]

C. Huttenhower, D. Gevers, R. Knight, et al., White, structure, function and diversity of the healthy human microbiome, Nature 486 (2012) 207-214. https://doi.org/10.1038/nature11234.
Crossref Google Scholar
[15]

M. Anitha, M. Vijay-Kumar, S.V. Sitaraman, et al., Gut microbial products regulate murine gastrointestinal motility via toll-like receptor 4 signaling, Gastroenterology. 143 (2012) 1006-1016. e4. https://doi.org/10.1053/j.gastro.2012.06.034.
Crossref Google Scholar
[16]

H. Neuman, J.W. Debelius, R. Knight, et al., Microbial endocrinology: the interplay between the microbiota and the endocrine system, FEMS Microbiol Rev. 39 (2015) 509-521. https://doi.org/10.1093/femsre/fuu010.
Crossref Google Scholar
[17]

J.G. LeBlanc, C. Milani, G.S. de Giori, et al., Bacteria as vitamin suppliers to their host: a gut microbiota perspective, Curr Opin Biotechnol. 24 (2013) 160-168. https://doi.org/10.1016/j.copbio.2012.08.005.
Crossref Google Scholar
[18]

H. Mineo, H. Hara, F. Tomita, Short-chain fatty acids enhance diffusional Ca transport in the epithelium of the rat cecum and colon, Life Sci. 69 (2001) 517-526. https://doi.org/10.1016/S0024-3205(01)01146-8.
Crossref Google Scholar
[19]

S.A. Bora, M.J. Kennett, P.B. Smith, et al., Regulation of vitamin D metabolism following disruption of the microbiota using broad spectrum antibiotics, J. Nutr. Biochem. 56 (2018) 65-73. https://doi.org/10.1016/j.jnutbio.2018.01.011.
Crossref Google Scholar
[20]

S.A. Bora, M.J. Kennett, P.B. Smith, et al., The gut microbiota regulates endocrine vitamin D metabolism through fibroblast growth factor 23, Front Immunol. 9 (2018) 1-11. https://doi.org/10.3389/fimmu.2018.00408.
Crossref Google Scholar
[21]

R. Krajmalnik-Brown, Z.E. Ilhan, D.W. Kang, J, et al., Effects of gut microbes on nutrient absorption and energy regulation, Nutr Clin Pract. 27(2012) 201-214. https://doi.org/10.1177/0884533611436116.
Crossref Google Scholar
[22]

C.N. Heiss, L.E. Olofsson, Gut microbiota-dependent modulation of energy metabolism, J. Innate. Immun. 10 (2018) 163-171. https://doi.org/10.1159/000481519.
Crossref Google Scholar
[23]

Y. Belkaid, T.W. Hand, Role of the microbiota in immunity and inflammation, Cell. 157 (2014) 121-141. https://doi.org/10.1016/j.cell.2014.03.011.
Crossref Google Scholar
[24]

M. Kriss, K.Z. Hazleton, N.M. Nusbacher, et al., Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery, Curr. Opin. Microbiol. 44 (2018) 34. https://doi.org/10.1016/J.MIB.2018.07.003.
Crossref Google Scholar
[25]

L. Crovesy, D. Masterson, L.E. Rosado, Profile of the gut microbiota of adults with obesity: a systematic review, Eur. J. Clin. Nutr. 74 (2020) 1251-1262. https://doi.org/10.1038/s41430-020-0607-6.
Crossref Google Scholar
[26]

T.R. Sampson, J.W. Debelius, T. Thron, et al., Gut microbiota regulate motor deficits and neuroinflammation in a model of parkinson's disease, Cell. 167(2016) 1469-1480. e12. https://doi.org/10.1016/j.cell.2016.11.018.
Crossref Google Scholar
[27]

E.Y. Hsiao, S.W. McBride, S. Hsien, et al., Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders, Cell. 155 (2013) 1451-1463. https://doi.org/10.1016/j.cell.2013.11.024.
Crossref Google Scholar
[28]

L. Coretti, L. Paparo, M.P. Riccio, et al., Gut microbiota features in young children with autism spectrum disorders, Front Microbiol. 9 (2018). https://doi.org/10.3389/fmicb.2018.03146.
Crossref Google Scholar
[29]

M.C. Dao, A. Everard, J. Aron-Wisnewsky, et al., Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: rela. pdf, Gut. 65 (2015) 426-36.
Crossref Google Scholar
[30]

S.M. Collins, A role for the gut microbiota in IBS, Nat. Rev. Gastroenterol Hepatol. 11 (2014) 497-505. https://doi.org/10.1038/nrgastro.2014.40.
Crossref Google Scholar
[31]

J. Wang, J. Qin, Y. Li, et al., A metagenome-wide association study of gut microbiota in type 2 diabetes, Nature 490 (2012) 55-60. https://doi.org/10.1038/nature11450.
Crossref Google Scholar
[32]

J. Peng, X. Xiao, M. Hu, et al., Interaction between gut microbiome and cardiovascular disease, Life Sci. 214 (2018) 153-157. https://doi.org/10.1016/j.lfs.2018.10.063.
Crossref Google Scholar
[33]

S. Zou, L. Fang, M.H. Lee, Dysbiosis of gut microbiota in promoting the development of colorectal cancer, Gastroenterol Rep (Oxf). 6 (2018) 1-12. https://doi.org/10.1093/gastro/gox031.
Crossref Google Scholar
[34]

K. Sjögren, C. Engdahl, P. Henning, et al., The gut microbiota regulates bone mass in mice, J. Bone Miner. Res. 27 (2012) 1357-1367. https://doi.org/10.1002/jbmr.1588.
Crossref Google Scholar
[35]

S. Carding, K. Verbeke, D.T. Vipond, et al., Dysbiosis of the gut microbiota in disease, Microb. Ecol. Health Dis. 26 (2015). https://doi.org/10.3402/mehd.v26.26191.
Crossref Google Scholar
[36]

M. Distefano, G. Veneto, S. Malservisi, et al., Small intestine bacterial overgrowth and metabolic bone disease, Dig. Dis. Sci. 46 (2001) 1077-1082. https://doi.org/10.1023/A:1010722314493.
Crossref Google Scholar
[37]

P. Stotzer, C. Johansson, D. Mellström, et al., Bone mineral density in patients with small intestinal bacterial overgrowth, Hepatogastroenterology. 50 (2003) 1415-1418.
Google Scholar
[38]

J. Yan, J.W. Herzog, K. Tsang, et al., Gut microbiota induce IGF-1 and promote bone formation and growth, Proc. Natl. Acad. Sci. U.S.A. 113 (2016) E7554-E7563. https://doi.org/10.1073/pnas.1607235113.
Crossref Google Scholar
[39]

M. Schwarzer, K. Makki, G. Storelli, et al., Lactobacillus plantarum strain maintains growth of infant mice during chronic undernutrition, Science 351(2016) 854-857. https://doi.org/10.1126/science.aad8588.
Crossref Google Scholar
[40]

A. Anantharaju, M. Klamut, Small intestinal bacterial overgrowth: A possible risk factor for metabolic bone disease, Nutr. Rev. 61 (2003) 132-135. https://doi.org/10.1301/nr.2003.apr.132-135.
Crossref Google Scholar
[41]

J.Y. Li, B. Chassaing, A.M. Tyagi, et al., Sex steroid deficiency-associated bone loss is microbiota dependent and prevented by probiotics, J. Clin. Investig. 126 (2016) 2049-2063. https://doi.org/10.1172/JCI86062.
Crossref Google Scholar
[42]

N. Wang, F. Meng, S. Ma, et al., Species-level gut microbiota analysis in ovariectomized osteoporotic rats by Shallow shotgun sequencing, Gene. 817(2022) 146205. https://doi.org/10.1016/j.gene.2022.146205.
Crossref Google Scholar
[43]

N. Wang, S. Ma, L. Fu, Gut microbiota dysbiosis as one cause of osteoporosis by impairing intestinal barrier function, Calcif. Tissue Int. 110(2022) 225-235. https://doi.org/10.1007/s00223-021-00911-7.
Crossref Google Scholar
[44]

M. Das, O. Cronin, D.M. Keohane, et al., Gut microbiota alterations associated with reduced bone mineral density in older adults, Rheumatology. 58 (2019) 2295-2304. https://doi.org/10.1093/rheumatology/kez302.
Crossref Google Scholar
[45]

C. Li, Q. Huang, R. Yang, et al., Gut microbiota composition and bone mineral loss-epidemiologic evidence from individuals in Wuhan, China, Osteoporos Int. 30 (2019) 1003-1013. https://doi.org/10.1007/s00198-019-04855-5.
Crossref Google Scholar
[46]

M. Wei, C. Li, Y. Dai, High-throughput absolute quantification sequencing revealed osteoporosis-related gut microbiota alterations in Han Chinese elderly, Front Cell Infect Microbiol. 11 (2021) 1-11. https://doi.org/10.3389/fcimb.2021.630372.
Crossref Google Scholar
[47]

Z. Xu, Z. Xie, J. Sun, Gut microbiome reveals specific dysbiosis in primary osteoporosis, Front Cell Infect Microbiol. 10 (2020) 1-12. https://doi.org/10.3389/fcimb.2020.00160.
Crossref Google Scholar
[48]

J. He, S. Xu, B. Zhang, Gut microbiota and metabolite alterations associated with reduced bone mineral density or bone metabolic indexes in postmenopausal osteoporosis, Aging. 12 (2020) 8583-8604. https://doi.org/10.18632/aging.103168.
Crossref Google Scholar
[49]

Y.W. Zhang, Y.J. Li, P.P. Lu, et al., The modulatory effect and implication of gut microbiota on osteoporosis: from the perspective of "brain-gut-bone" axis, Food Funct. (2021). https://doi.org/10.1039/d0fo03468a.
Crossref Google Scholar
[50]

D. Ozaki, R. Kubota, T. Maeno, et al., Association between gut microbiota, bone metabolism, and fracture risk in postmenopausal Japanese women, Osteoporos Int. 32 (2021) 145-156. https://doi.org/10.1007/s00198-020-05728-y.
Crossref Google Scholar
[51]

M. Das, O. Cronin, D.M. Keohane, et al., Gut microbiota alterations associated with reduced bone mineral density in older adults, Rheumatology. 58 (2019) 2295-2304. https://doi.org/10.1093/rheumatology/kez302.
Crossref Google Scholar
[52]

J. Cheng, W.L. Zhong, J.W. Zhao, et al., Alterations in the composition of the gut microbiota affect absorption of cholecalciferol in severe osteoporosis, J. Bone Miner. Metab. 40 (2022) 478-486. https://doi.org/10.1007/S00774-021-01303-5/FIGURES/4.
Crossref Google Scholar
[53]

C. Palacios, The role of nutrients in bone health, from A to Z, Crit Rev Food Sci. Nutr. 46 (2006) 621-628. https://doi.org/10.1080/10408390500466174.
Crossref Google Scholar
[54]

D.M. Hegsted, Calcium and osteoporosis?, Adv Nutr Res. 9 (1994) 119-128.
Crossref Google Scholar
[55]

T.C. Wallace, M. Marzorati, L. Spence, et al., New frontiers in fibers: Innovative and emerging research on the gut microbiome and bone health, J. Am. Coll Nutr. 36 (2017) 218-222. https://doi.org/10.1080/07315724.2016.1257961.
Crossref Google Scholar
[56]

S. Tedelind, F. Westberg, M. Kjerrulf, et al., Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease, World J. Gastroenterol. 13 (2007) 2826. https://doi.org/10.3748/WJG.V13.I20.2826.
Crossref Google Scholar
[57]
E. Hijová, A. Chmelarova, Short chain fatty acids and colonic health, (2007). https://www.researchgate.net/publication/5647158 (accessed June 22, 2022).
[58]

F. Liu, J. Li, F. Wu, et al., Altered composition and function of intestinal microbiota in autism spectrum disorders: a systematic review, Transl Psychiatry. 9 (2019). https://doi.org/10.1038/s41398-019-0389-6.
Crossref Google Scholar
[59]

K. Hiippala, H. Jouhten, A. Ronkainen, et al., The potential of gut commensals in reinforcing intestinal barrier function and alleviating inflammation, Nutrients 10 (2018) 988. https://doi.org/10.3390/NU10080988.
Crossref Google Scholar
[60]

P. Van Den Abbeele, C. Belzer, M. Goossens, et al., Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model, ISME Journal. 7 (2013) 949-961. https://doi.org/10.1038/ismej.2012.158.
Crossref Google Scholar
[61]

J.B. Lian, G.S. Stein, Vitamin D regulation of osteoblast growth and differentiation, Nutrition and Gene Expression. (2018) 391-429. https://doi.org/10.1201/9781351075114-18.
Crossref Google Scholar
[62]

P. Lips, N.M. van Schoor, The effect of vitamin D on bone and osteoporosis, Best Pract. Res. Clin. Endocrinol Metab. 25 (2011) 585-591. https://doi.org/10.1016/J.BEEM.2011.05.002.
Crossref Google Scholar
[63]

S. Ruiz-Gaspà, N. Guañabens, A. Enjuanes, et al., Lithocholic acid downregulates vitamin D effects in human osteoblasts, Eur. J. Clin. Invest. 40 (2010) 25-34. https://doi.org/10.1111/j.1365-2362.2009.02230.x.
Crossref Google Scholar
[64]

S.W. Cho, J.H. An, H. Park, et al., Positive regulation of osteogenesis by bile acid through FXR, J. Bone Miner. Res. 28 (2013) 2109-2121. https://doi.org/10.1002/jbmr.1961.
Crossref Google Scholar
[65]

J. Wu, D.E. Shang, S. Yang, et al., Association between the vitamin D receptor gene polymorphism and osteoporosis, Biomed Rep. 5 (2016) 233-236. https://doi.org/10.3892/br.2016.697.
Crossref Google Scholar
[66]

W. He, M. Liu, X. Huang, et al., The influence of vitamin D receptor genetic variants on bone mineral density and osteoporosis in chinese postmenopausal women, Dis. Markers. (2015) https://doi.org/10.1155/2015/760313.
Crossref Google Scholar
[67]

M. Kow, E. Akam, P. Singh, et al., Vitamin D receptor (VDR) gene polymorphism and osteoporosis risk in White British men, Ann. Hum. Biol. 46 (2019) 430-433. https://doi.org/10.1080/03014460.2019.1659851.
Crossref Google Scholar
[68]

M. Bashir, B. Prietl, M. Tauschmann, et al., Effects of high doses of vitamin D3 on mucosa-associated gut microbiome vary between regions of the human gastrointestinal tract, Eur. J. Nutr. 55 (2016) 1479-1489. https://doi.org/10.1007/s00394-015-0966-2.
Crossref Google Scholar
[69]

M.S. Hamidi, O. Gajic-Veljanoski, A.M. Cheung, Vitamin K and bone health, J. Clin. Densitom. 16 (2013) 409-413. https://doi.org/10.1016/j.jocd.2013.08.017.
Crossref Google Scholar
[70]

J.K.D. Villa, M.A.N. Diaz, V.R. Pizziolo, et al., Effect of vitamin K in bone metabolism and vascular calcification: A review of mechanisms of action and evidence, Crit. Rev. Food Sci. Nutr. 57 (2017) 3959-3970. https://doi.org/10.1080/10408398.2016.1211616.
Crossref Google Scholar
[71]

D. Ulluwishewa, R.C. Anderson, W.C. McNabb, et al., Regulation of tight junction permeability by intestinal bacteria and dietary components, J. Nutr. 141 (2011) 769-776. https://doi.org/10.3945/jn.110.135657.
Crossref Google Scholar
[72]

G. Qi. Hou, C. Guo, G.H. Song, et al., Lipopolysaccharide (LPS) promotes osteoclast differentiation and activation by enhancing the MAPK pathway and COX-2 expression in RAW264.7 cells, Int. J. Mol. Med. 32 (2013) 503-510. https://doi.org/10.3892/ijmm.2013.1406.
Crossref Google Scholar
[73]

H. Kadono, J.I. Kido, M. Kataoka, et al., Inhibition of osteoblastic cell differentiation by lipopolysaccharide extract from Porphyromonas gingivalis, Infect Immun. 67(1999) 2841-2846. https://doi.org/10.1128/iai.67.6.2841-2846.1999.
Crossref Google Scholar
[74]

A. di Benedetto, I. Gigante, S. Colucci, et al., Periodontal disease: linking the primary inflammation to bone loss, Clin. Dev. Immunol. 2013 (2013) 1-7. https://doi.org/10.1155/2013/503754.
Crossref Google Scholar
[75]

O. Kudo, A. Sabokbar, A. Pocock, et al., Interleukin-6 and interleukin-11 support human osteoclast formation by a RANKL-independent mechanism, Bone. 32 (2003) 1-7. https://doi.org/10.1016/S8756-3282(02)00915-8.
Crossref Google Scholar
[76]

P.P.C. Souza, U.H. Lerner, The role of cytokines in inflammatory bone loss, Immunol. Invest. 42 (2013) 555-622. https://doi.org/10.3109/08820139.2013.822766.
Crossref Google Scholar
[77]

K. Itoh, N. Udagawa, K. Kobayashi, et al., Lipopolysaccharide promotes the survival of osteoclasts via toll-like receptor 4, but cytokine production of osteoclasts in response to lipopolysaccharide is different from that of macrophages, J. Immunol. 170 (2003) 3688-3695. https://doi.org/10.4049/jimmunol.170.7.3688.
Crossref Google Scholar
[78]

P.B. Eckburg, E.M. Bik, C.N. Bernstein, et al., Microbiology: diversity of the human intestinal microbial flora, Science 308 (2005) 1635-1638. https://doi.org/10.1126/science.1110591.
Crossref Google Scholar
[79]

Y. Abu-Amer, F.P. Ross, J. Edwards, et al., Lipopolysaccharide-stimulated osteoclastogenesis is mediated by tumor necrosis factor via its P55 receptor, J. Clin. Investig. 100 (1997) 1557-1565. https://doi.org/10.1172/JCI119679.
Crossref Google Scholar
[80]

M. Mörmann, M. Thederan, I. Nackchbandi, et al., Lipopolysaccharides (LPS) induce the differentiation of human monocytes to osteoclasts in a tumour necrosis factor (TNF) α-dependent manner: a link between infection and pathological bone resorption, Mol. Immunol. 45 (2008) 3330-3337. https://doi.org/10.1016/j.molimm.2008.04.022.
Crossref Google Scholar
[81]

T.R. Sponholtz, X. Zhang, J.D.T. Fontes, et al., Association between inflammatory biomarkers and bone mineral density in a community-based cohort of men and women, Arthritis. Care. Res. (Hoboken). 66 (2014) 1233-1240. https://doi.org/10.1002/acr.22270.
Crossref Google Scholar
[82]

C. Scheidt-Nave, H. Bismar, G. Leidig-Bruckner, et al., Serum interleukin 6 is a major predictor of bone loss in women specific to the first decade past menopause, J. Clin. Endocrinol. Metab. 86 (2001) 2032-2042. https://doi.org/10.1210/jc.86.5.2032.
Crossref Google Scholar
[83]

M. Rescigno, Intestinal microbiota and its effects on the immune system, Cell Microbiol. 16 (2014) 1004-1013. https://doi.org/10.1111/cmi.12301.
Crossref Google Scholar
[84]

L. Macia, A.N. Thorburn, L.C. Binge, et al., Microbial influences on epithelial integrity and immune function as a basis for inflammatory diseases, Immunol Rev. 245 (2012) 164-176. https://doi.org/10.1111/j.1600-065X.2011.01080.x.
Crossref Google Scholar
[85]

A. Kassem, P. Henning, B. Kindlund, et al., TLR5, a novel mediator of innate immunity-induced osteoclastogenesis and bone loss, FASEB J. 29(2015) 4449-4460. https://doi.org/10.1096/fj.15-272559.
Crossref Google Scholar
[86]

J.A. Chaves de Souza, Sa. C.T. Frasnelli, F. de A. Curylofo-Zotti, et al., NOD1 in the modulation of host-microbe interactions and inflammatory bone resorption in the periodontal disease model, Immunology. 149 (2016) 374-385. https://doi.org/10.1111/imm.12654.
Crossref Google Scholar
[87]

L. Li, S. Rao, Y. Cheng, et al., Microbial osteoporosis: the interplay between the gut microbiota and bones via host metabolism and immunity, Microbiologyopen. 8 (2019) 1-15. https://doi.org/10.1002/mbo3.810.
Crossref Google Scholar
[88]

C. Li, G. Pi, F. Li, The role of intestinal flora in the regulation of bone homeostasis, Front Cell Infect. Microbiol. 11 (2021) 1-16. https://doi.org/10.3389/fcimb.2021.579323.
Crossref Google Scholar
[89]

T.P. Prates, T.M. Taira, M.C. Holanda, et al., NOD2 contributes to porphyromonas gingivalis-induced bone resorption, J. Dent. Res. 93 (2014) 1155-1162. https://doi.org/10.1177/0022034514551770.
Crossref Google Scholar
[90]

K. Sato, A. Suematsu, K. Okamoto, et al., Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction, J. Exp. Med. 203 (2006) 2673-2682. https://doi.org/10.1084/JEM.20061775.
Crossref Google Scholar
[91]

M. Yu, S. Pal, C.W. Paterson, et al., Ovariectomy induces bone loss via microbial-dependent trafficking of intestinal TNF+T cells and Th17 cells, J. Clin. Investig. 131 (2021) 1-13. https://doi.org/10.1172/JCI143137.
Crossref Google Scholar
[92]

S. Kotake, N. Udagawa, N. Takahashi, et al., Suda, IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis, J. Clin. Investig. 103 (1999) 1345-1352. https://doi.org/10.1172/JCI5703.
Crossref Google Scholar
[93]

J. Lam, S. Takeshita, J.E. Barker, et al., TNF-α induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand, J. Clin. Investig. 106 (2000) 1481-1488. https://doi.org/10.1172/JCI11176.
Crossref Google Scholar
[94]

Y. Gao, F. Grassi, M.R. Ryan, et al., IFN-γ stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation, J. Clin. Investig. 117 (2007) 122-132. https://doi.org/10.1172/JCI30074.
Crossref Google Scholar
[95]

Y.Y. Kong, U. Felge, I. Sarosi, et al., Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand, Nature 402 (1999) 304-309. https://doi.org/10.1038/46303.
Crossref Google Scholar
[96]

K. Sato, A. Suematsu, K. Okamoto, et al., Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction, J. Exp. Med. 203 (2006) 2673-2682. https://doi.org/10.1084/jem.20061775.
Crossref Google Scholar
[97]

I.I. Ivanov, K. Atarashi, N. Manel, et al., Induction of intestinal Th17 Cells by segmented filamentous bacteria, Cell. 139 (2009) 485-498. https://doi.org/10.1016/j.cell.2009.09.033.
Crossref Google Scholar
[98]

M.M. Zaiss, K. Sarter, A. Hess, et al., Increased bone density and resistance to ovariectomy-induced bone loss in FoxP3-transgenic mice based on impaired osteoclast differentiation, Arthritis Rheum. 62 (2010) 2328-2338. https://doi.org/10.1002/art.27535.
Crossref Google Scholar
[99]

A.M. Tyagi, M. Yu, T.M. Darby, et al., The microbial metabolite butyrate stimulates bone formation via T regulatory cell-mediated regulation of WNT10B expression, Immunity. 49 (2018) 1116-1131. e7. https://doi.org/10.1016/j.immuni.2018.10.013.
Crossref Google Scholar
[100]

P.M. Smith, M.R. Howitt, N. Panikov, et al., The microbial metabolites, short-chain fatty acids, regulate colonic T reg cell homeostasis, Science(1979). 341 (2013) 569-573. https://doi.org/10.1126/science.1241165/suppl_file/smith.sm.revision.1.pdf.
Crossref Google Scholar
[101]

Y. Furusawa, Y. Obata, S. Fukuda, et al., Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells, Nature 504 (2013) 446-450. https://doi.org/10.1038/nature12721.
Crossref Google Scholar
[102]

K. Atarashi, T. Tanoue, T. Shima, et al., Induction of colonic regulatory T cells by indigenous Clostridium species, Science (1979). 331 (2011) 337-341. https://doi.org/10.1126/science.1198469/suppl_file/atarashi_som.pdf.
Crossref Google Scholar
[103]

M.D. Gershon, J. Tack, The serotonin signaling system: From basic understanding to drug development for functional GI disorders, Gastroenterology. 132 (2007) 397-414. https://doi.org/10.1053/j.gastro.2006.11.002.
Crossref Google Scholar
[104]

B. Lavoie, J.A. Roberts, M.M. Haag, et al., Gut-derived serotonin contributes to bone deficits in colitis, Pharmacol Res. 140 (2019) 75-84. https://doi.org/10.1016/J.PHRS.2018.07.018.
Crossref Google Scholar
[105]

H.L. Kristjansdottir, C. Lewerin, U.H. Lerner, et al., High serum serotonin predicts increased risk for hip fracture and nonvertebral osteoporotic fractures: The MrOS Sweden Study, J. Bone Miner. Res. 33 (2018) 1560-1567. https://doi.org/10.1002/JBMR.3443.
Crossref Google Scholar
[106]

U.I. Mödder, S.J. Achenbach, S. Amin, et al., Relation of serum serotonin levels to bone density and structural parameters in women, J. Bone Miner. Res. 25 (2010) 415-422. https://doi.org/10.1359/JBMR.090721.
Crossref Google Scholar
[107]
P. Ducy, G. Karsenty, The two faces of serotonin in bone biology, 191 (2010). https://doi.org/10.1083/jcb.201006123.
Crossref
[108]

D.J. Walther, J.U. Peter, S. Bashammakh, et al., Synthesis of serotonin by a second tryptophan hydroxylase isoform, Science (1979). 299 (2003) 76. https://doi.org/10.1126/science.1078197.
Crossref Google Scholar
[109]

F. Côté, E. Thévenot, C. Fligny, et al., Disruption of the nonneuronal tph1 gene demonstrates the importance of peripheral serotonin in cardiac function, Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 13525-13530. https://doi.org/10.1073/pnas.2233056100.
Crossref Google Scholar
[110]

J.M. Yano, K. Yu, G.P. Donaldson, et al., Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis, Cell. 161 (2015) 264-276. https://doi.org/10.1016/j.cell.2015.02.047.
Crossref Google Scholar
[111]

M. Bliziotes, A. Eshleman, B. Burt-Pichat, et al., Serotonin transporter and receptor expression in osteocytic MLO-Y4 cells, Bone. 39 (2006) 1313-1321. https://doi.org/10.1016/j.bone.2006.06.009.
Crossref Google Scholar
[112]

V.K. Yadav, S. Balaji, P.S. Suresh, et al., Pharmacological inhibition of gut-derived serotonin synthesis is a potential bone anabolic treatment for osteoporosis, Nat. Med. 16 (2010) 308-312. https://doi.org/10.1038/nm.2098.
Crossref Google Scholar
[113]

Y. Chabbi-Achengli, A.E. Coudert, J. Callebert et al., Decreased osteoclastogenesis in serotonin-deficient mice, Proc. Natl. Acad. Sci. U.S.A. 109 (2012) 2567-2572. https://doi.org/10.1073/pnas.1117792109.
Crossref Google Scholar
[114]
L.R. McCabe, Understanding the gut-bone signaling axis, 2017. https://doi.org/10.1007/978-3-319-66653-2.
Crossref
[115]

F. Zhang, Y. Chen, M. Heiman, et al., Leptin: structure, function and biology, Vitam. Horm. 71 (2005) 345-372. https://doi.org/10.1016/S0083-6729(05)71012-8.
Crossref Google Scholar
[116]

Y. Charnay, I. Cusin, P.G. Vallet, et al., Intracerebroventricular infusion of leptin decreases serotonin transporter binding sites in the frontal cortex of the rat, Neurosci. Lett. 283 (2000) 89-92. https://doi.org/10.1016/S0304-3940(00)00951-4.
Crossref Google Scholar
[117]

V.K. Yadav, F. Oury, N. Suda, Z et al., A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure, Cell. 138 (2009) 976-989. https://doi.org/10.1016/j.cell.2009.06.051.
Crossref Google Scholar
[118]

M.I. Queipo-Ortuño, L.M. Seoane, M. Murri, et al., Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels, PLoS One 8(2013). https://doi.org/10.1371/journal.pone.0065465.
Crossref Google Scholar
[119]

J.Y. Li, M. Yu, S. Pal, et al., Parathyroid hormone-dependent bone formation requires butyrate production by intestinal microbiota, J. Clin. Investig. 130(2020) 1767-1781. https://doi.org/10.1172/JCI133473.
Crossref Google Scholar
[120]

M.A. Avella, A. Place, S.J. Du, et al., Lactobacillus rhamnosus accelerates zebrafish backbone calcification and gonadal differentiation through effects on the GnRH and IGF systems, PLoS One 7 (2012) 1-10. https://doi.org/10.1371/journal.pone.0045572.
Crossref Google Scholar
[121]

S.C. Shin, S.H. Kim, H. You, et al., Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling, Science(1979). 334 (2011) 670-674. https://doi.org/10.1126/science.1212782.
Crossref Google Scholar
[122]

G. Storelli, A. Defaye, B. Erkosar, et al., Lactobacillus plantarum promotes drosophila systemic growth by modulating hormonal signals through TORdependent nutrient sensing, Cell Metab. 14 (2011) 403-414. https://doi.org/10.1016/j.cmet.2011.07.012.
Crossref Google Scholar
[123]

B.Y. Reed, J.E. Zerwekh, K. Sakhaee, et al., Serum IGF 1 is low and correlated with osteoblastic surface in idiopathic osteoporosis, J. Bone Miner. Res. 10 (1995) 1218-1224. https://doi.org/10.1002/jbmr.5650100812.
Crossref Google Scholar
[124]

J. Yan, J.W. Herzog, K. Tsang, et al., Gut microbiota induce IGF-1 and promote bone formation and growth, Proc. Natl. Acad. Sci. U.S.A. 113 (2016) E7554-E7563. https://doi.org/10.1073/pnas.1607235113.
Crossref Google Scholar
[125]

J. Yan, A. Takakura, K. Zandi-Nejad, et al., Mechanisms of gut microbiotamediated bone remodeling, Gut Microbes. 9 (2018) 84-92. https://doi.org/10.1080/19490976.2017.1371893.
Crossref Google Scholar
[126]

J. Yan, J.F. Charles, Gut microbiota and IGF-1, Calcif Tissue Int. 102 (2018) 406-414. https://doi.org/10.1007/s00223-018-0395-3.
Crossref Google Scholar
[127]

F. Albright, P. Smith, A. Richardson, Post menopausal osteoporosis: its clinical features, JAMA. 116 (1941) 2465-2474.
Crossref Google Scholar
[128]

C.S. Plottel, M.J. Blaser, Microbiome and malignancy, Cell Host Microbe. 10 (2011) 324-335. https://doi.org/10.1016/j.chom.2011.10.003.
Crossref Google Scholar
[129]

J.M. Baker, L. Al-Nakkash, M.M. Herbst-Kralovetz, Estrogen-gut microbiome axis: Physiological and clinical implications, Maturitas. 103(2017) 45-53. https://doi.org/10.1016/j.maturitas.2017.06.025.
Crossref Google Scholar
[130]

M. Kwa, C.S. Plottel, M.J. Blaser, et al., The intestinal microbiome and estrogen receptor-positive female breast cancer, J. Natl. Cancer Inst. 108(2016) 1-10. https://doi.org/10.1093/jnci/djw029.
Crossref Google Scholar
[131]

V. Blasco-Baque, M. Serino, J.N. Vergnes, et al., High-fat diet induces periodontitis in mice through lipopolysaccharides (LPS) receptor signaling: Protective action of estrogens, PLoS One 7 (2012) 1-12. https://doi.org/10.1371/journal.pone.0048220.
Crossref Google Scholar
[132]

J.A. Spanier, F.E. Nashold, C.G. Mayne, et al., Vitamin D and estrogen synergy in Vdr-expressing CD4+T cells is essential to induce Helios+FoxP3+T cells and prevent autoimmune demyelinating disease, J. Neuroimmunol. 286 (2015) 48-58. https://doi.org/10.1016/j.jneuroim.2015.06.015.
Crossref Google Scholar
[133]

E. Seeman, T.J. Martin, Antiresorptive and anabolic agents in the prevention and reversal of bone fragility, Nat Rev Rheumatol. 15 (2019) 225-236. https://doi.org/10.1038/s41584-019-0172-3.
Crossref Google Scholar
[134]

S. Khosla, R. Pacifici, Estrogen deficiency, postmenopausal osteoporosis, and age-related bone loss, Fourth Edi, Elsevier, 2013. https://doi.org/10.1016/B978-0-12-415853-5.00046-7.
Crossref Google Scholar
[135]

A.M. Pack, Anticonvulsant-related bone disease, Fourth Edi, Elsevier, 2013. https://doi.org/10.1016/B978-0-12-415853-5.00050-9.
Crossref Google Scholar
[136]

C. Hill, F. Guarner, G. Reid, et al., 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 (2014) 506-514. https://doi.org/10.1038/nrgastro.2014.66.
Crossref Google Scholar
[137]

L.R. Mccabe, R. Irwin, L. Schaefer, et al., Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice, J. Cell Physiol. 228 (2013) 1793-1798. https://doi.org/10.1002/jcp.24340.
Crossref Google Scholar
[138]

R.A. Britton, R. Irwin, D. Quach, et al., Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse Model, J. Cell Physiol. 229 (2014) 1822-1830. https://doi.org/10.1002/jcp.24636.
Crossref Google Scholar
[139]

J. Zhang, K.J. Motyl, R. Irwin, et al., Loss of bone and Wnt10b expression in male type 1 diabetic mice is blocked by the probiotic Lactobacillus reuteri, Endocrinology. 156 (2015) 3169-3182. https://doi.org/10.1210/EN.2015-1308.
Crossref Google Scholar
[140]

J.D. Schepper, F. Collins, N.D. Rios-Arce, et al., Involvement of the gut microbiota and barrier function in glucocorticoid-induced osteoporosis, J. Bone Miner. Res. 35 (2020) 801-820. https://doi.org/10.1002/jbmr.3947.
Crossref Google Scholar
[141]

A.G. Nilsson, D. Sundh, F. Bäckhed, et al., Lactobacillus reuteri reduces bone loss in older women with low bone mineral density: a randomized, placebo-controlled, double-blind, clinical trial, J. Intern. Med. 284 (2018) 307-317. https://doi.org/10.1111/joim.12805.
Crossref Google Scholar
[142]

C. Ohlsson, C. Engdahl, F. Fak, et al., Probiotics protect mice from ovariectomy-induced cortical bone loss, PLoS One. 9 (2014). https://doi.org/10.1371/journal.pone.0092368.
Crossref Google Scholar
[143]

T. Maekawa, G. Hajishengallis, Topical treatment with probiotic Lactobacillus brevis CD2 inhibits experimental periodontal inflammation and bone loss, J. Periodontal Res. 49 (2014) 785-791. https://doi.org/10.1111/JRE.12164.
Crossref Google Scholar
[144]

N. Montazeri-Najafabady, Y. Ghasemi, M.H. Dabbaghmanesh, et al., Supportive role of probiotic strains in protecting rats from ovariectomyinduced cortical bone loss, Probiotics Antimicrob Proteins. 11 (2019) 1145-1154. https://doi.org/10.1007/S12602-018-9443-6/FIGURES/4.
Crossref Google Scholar
[145]

M.L. Jones, C.J. Martoni, S. Prakash, Oral supplementation with probiotic L. reuteri NCIMB 30242 increases mean circulating 25-hydroxyvitamin D: a post hoc analysis of a randomized controlled trial, J. Clin. Endocrinol Metab. 98 (2013) 2944-2951. https://doi.org/10.1210/JC.2012-4262.
Crossref Google Scholar
[146]

K. Parvaneh, M. Ebrahimi, M.R. Sabran, 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(2015). https://doi.org/10.1155/2015/897639.
Crossref Google Scholar
[147]

F. Ca. Rodrigues, A.S.B. Castro, V.C. Rodrigues, et al., Yacon flour and Bifidobacterium longum modulate bone health in rats, J. Med. Food. 15(2012) 664-670. https://doi.org/10.1089/jmf.2011.0296.
Crossref Google Scholar
[148]

H. Lan, W.H. Liu, H. Zheng, et al., Bifidobacterium lactis BL-99 protects mice with osteoporosis caused by colitis via gut inflammation and gut microbiota regulation, Food Funct. 13 (2022) 1482-1494. https://doi.org/10.1039/D1FO02218K.
Crossref Google Scholar
[149]

D.E. Kim, J.K. Kim, S.K. Han, et al., 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. 22(2019) 1022-1031. https://doi.org/10.1089/jmf.2019.4419.
Crossref Google Scholar
[150]

S. Yuan, J. Shen, Bacteroides vulgatus diminishes colonic microbiota dysbiosis ameliorating lumbar bone loss in ovariectomized mice, Bone. 142(2021) 115710. https://doi.org/10.1016/j.bone.2020.115710.
Crossref Google Scholar
[151]

M. Hatanaka, T. Hoshino, K. Tanaka, et al., Effect of Bacillus subtilis C-3102 on bone mineral density in healthy double-blind clinical trial Takuou TAKIMOTO, Biosci Microbiota Food Health. (2018).
Google Scholar
[152]

G.R. Gibson, R. Hutkins, M.E. Sanders, et al., The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics, Nat Rev Gastroenterol Hepatol. 14(2017). https://doi.org/10.1038/s41575-021-00440-6.
Crossref Google Scholar
[153]

Y. Bouhnik, L. Raskine, G. Simoneau, et al., The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a doubleblind, randomized, placebo-controlled, parallel-group, dose-response relation study, Am. J. Clin. Nutri. 80 (2004) 1658-1664. https://doi.org/10.1093/ajcn/80.6.1658.
Crossref Google Scholar
[154]

O. Chonan, K. Matsumoto, M. Watanuki, Effect of galactooligosaccharides on calcium absroption and preventing bone loss in ovariectomized rats, Chemical Pharmaceutical Bulletin. 17 (1994) 1460-1462.
Crossref Google Scholar
[155]

C.M. Weaver, B.R. Martin, C.H. Nakatsu, et al., Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation, J. Agric. Food Chem. 59 (2011) 6501-6510. https://doi.org/10.1021/jf2009777.
Crossref Google Scholar
[156]

E.G.H.M. Van Den Heuvel, M.H.C. Schoterman, T. Muijs, Transgalactooligosaccharides stimulate calcium absorption in postmenopausal women, J. Nutr. 130 (2000) 2938-2942. https://doi.org/10.1093/jn/130.12.2938.
Crossref Google Scholar
[157]

S.A. Jakeman, C.N. Henry, B.R. Martin, et al., Soluble corn fiber increases bone calcium retention in postmenopausal women in a dose-dependent manner: A randomized crossover trial, Am. J. Clin. Nutr. 104 (2016) 837-843. https://doi.org/10.3945/ajcn.116.132761.
Crossref Google Scholar
[158]

M. Dolores Tenorio, I. Espinosa-Martos, G. Préstamo, et al., Soybean whey enhance mineral balance and caecal fermentation in rats, Eur. J. Nutr. 49(2010) 155-163. https://doi.org/10.1007/s00394-009-0060-8.
Crossref Google Scholar
[159]

L. Raschka, H. Daniel, Mechanisms underlying the effects of inulin-type fructans on calcium absorption in the large intestine of rats, Bone. 37 (2005) 728-735. https://doi.org/10.1016/j.bone.2005.05.015.
Crossref Google Scholar
[160]

L. Holloway, S. Moynihan, S.A. Abrams, et al., Effects of oligofructoseenriched inulin on intestinal absorption of calcium and magnesium and bone turnover markers in postmenopausal women, British J. Nutr. 97 (2007) 365-372. https://doi.org/10.1017/S000711450733674X.
Crossref Google Scholar
[161]

M. De Vrese, J. Schrezenmeir, Probiotics, prebiotics, and synbiotics, Adv Biochem Engin/Biotechnol. 111 (2008) 1-66. https://doi.org/10.1007/10_2008_097.
Crossref Google Scholar
[162]

D. Pérez-Conesa, G. Lopez, P. Abellan, et al., Bioavailability of calcium, magnesiumand phosphorus in rats fed probiotic, prebiotic and synbiotic powder follow-upinfant formulas and their effect on physiological and nutritional parameters, J. Sci. Food Agric. 1243 (2006) 2327-2336. https://doi.org/10.1002/jsfa.
Crossref Google Scholar
[163]

D. Pérez-Conesa, G. Lopez, G. Ros, Effects of probiotic, prebiotic and synbiotic follow-up infant formulas on large intestine morphology and bone mineralisation in rats, J. Sci. Food Agric. 87 (2007) 1059-1068. https://doi.org/10.1002/jsfa.2812.
Crossref Google Scholar
[164]

B. Adolphi, K.E. Scholz-Ahrens, M. de Vrese, et al., Short-term effect of bedtime consumption of fermented milk supplemented with calcium, inulin-type fructans and caseinphosphopeptides on bone metabolism in healthy, postmenopausal women, Eur. J. Nutr. 48 (2009) 45-53. https://doi.org/10.1007/s00394-008-0759-y.
Crossref Google Scholar
[165]

M.L. Marco, M.E. Sanders, M. Gänzle, et al., The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on fermented foods, Nat Rev Gastroenterol Hepatol. 18 (2021) 196-208. https://doi.org/10.1038/s41575-020-00390-5.
Crossref Google Scholar
[166]

S.S. Chiang, T.M. Pan, 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 (2011) 7734-7742. https://doi.org/10.1021/jf2013716.
Crossref Google Scholar
[167]

C.S. Lee, S.H. Lee, S.H. Kim, Bone-protective effects of Lactobacillus plantarum B719-fermented milk product, Int. J. Dairy Technol. 73 (2020) 706-717. https://doi.org/10.1111/1471-0307.12701.
Crossref Google Scholar
[168]

M. Narva, J. Halleen, K. Väänänen, et al., Effects of Lactobacillus helveticus fermented milk on bone cells in vitro, Life Sci. 75 (2004) 1727-1734. https://doi.org/10.1016/j.lfs.2004.04.011.
Crossref Google Scholar
[169]

M. Narva, R. Nevala, T. Poussa, et al., The effect of Lactobacillus helveticus fermented milk on acute changes in calcium metabolism in postmenopausal women, Eur. J. Nutr. 43 (2004) 61-68. https://doi.org/10.1007/s00394-004-0441-y.
Crossref Google Scholar
[170]

M. Narva, M. Collin, T. Jauhiainen, et al., Effects of Lactobacillus helveticus fermented milk and its bioactive peptides on bone parameters in spontaneously hypertensive rats, Milchwissenschaft. 59 (2004) 359-363.
Google Scholar
[171]

Y.Manios, G.Moschonis, K.Koutsikas, et al., Changes in body composition following a dietary and lifestyle intervention trial: the postmenopausal health study, Maturitas.62 (2009) 58-65.https://doi.org/10.1016/j.maturitas.2008.11.005.
Crossref Google Scholar
[172]

Y. Manios, G. Moschonis, G. Trovas, et al., Changes in biochemical indexes of bone metabolism and bone mineral density after a 12-mo dietary intervention program: the postmenopausal health Study, Am. J. Clin. Nutr.86 (2007) 781-789. https://doi.org/10.1093/ajcn/86.3.781.
Crossref Google Scholar
[173]

G. Moschonis, S. Kanellakis, N. Papaioannou, et al., Possible site-specific effect of an intervention combining nutrition and lifestyle counselling with consumption of fortified dairy products on bone mass: the postmenopausal health study Ⅱ, J. Bone Miner. Metab. 29 (2011) 501-506. https://doi.org/10.1007/S00774-010-0256-2/TABLES/2.
Crossref Google Scholar
[174]

G. Moschonis, I. Katsaroli, G.P. Lyritis, et al., The effects of a 30-month dietary intervention on bone mineral density: the postmenopausal health study, British Journal of Nutrition. 104 (2010) 100-107. https://doi.org/10.1017/S000711451000019X.
Crossref Google Scholar
[175]

G. Moschonis, Y. Manios, Skeletal site-dependent response of bone mineral density and quantitative ultrasound parameters following a 12-month dietary intervention using dairy products fortified with calcium and vitamin D: the Postmenopausal Health Study, Br. J. Nutr. 96 (2006) 1140-1148. https://doi.org/10.1017/BJN20061977.
Crossref Google Scholar
[176]

J.-P. Bonjour, V. Benoit, O. Pourchaire, et al., Nutritional approach for inhibiting bone resorption in institutionalized elderly women with vitamin D insufficiency and high prevalence of fracture, J. Nutr. Health Aging. 15(2011) 404-409. https://doi.org/10.1007/s12603-011-0003-y.
Crossref Google Scholar
[177]

M.Y. Tu, K.Y. Han, G.R.L. Chang, et al., Kefir peptides prevent estrogen deficiency-induced bone loss and modulate the structure of the gut microbiota in ovariectomized mice, Nutrients. 12 (2020) 3432. https://doi.org/10.3390/nu12113432.
Crossref Google Scholar
[178]

M. Moazen, Z. Mazloom, N. Tanideh, et al., Osteoprotective effects of kefir fortified with omega-3 and vitamin C in ovariectomized rats, Int J Vitam Nutr Res, (2021) (2021). https://doi.org/10.1024/0300-9831/A000718.
Crossref Google Scholar
[179]

Y. Ikeda, M. Iki, A. Morita, et al., Intake of fermented soybeans, natto, is associated with reduced bone loss in postmenopausal women: japanese population-based osteoporosis (JPOS) study, J. Nutr. 136 (2006) 1323-1328. https://doi.org/10.1093/jn/136.5.1323.
Crossref Google Scholar
[180]

A. Kojima, S. Ikehara, K. Kamiya, et al., Natto intake is inversely associated with osteoporotic fracture risk in postmenopausal Japanese Women, J Nutr. 150 (2020) 599-605. https://doi.org/10.1093/jn/nxz292.
Crossref Google Scholar
[181]

H. Katsuyama, S. Ideguchi, M. Fukunaga, et al., Promotion of bone formation by fermented soybean (Natto) intake in premenopausal women, J. Nutr. Sci. Vitaminol (Tokyo). 50 (2004) 114-120. https://doi.org/10.3177/jnsv.50.114.
Crossref Google Scholar
[182]

S. Shin, H. Joung, A dairy and fruit dietary pattern is associated with a reduced likelihood of osteoporosis in Korean postmenopausal women, Br. J. Nutr. 110 (2013) 1926-1933. https://doi.org/10.1017/S0007114513001219.
Crossref Google Scholar
[183]

S. Shin, J. Sung, H. Joung, A fruit, milk and whole grain dietary pattern is positively associated with bone mineral density in Korean healthy adults, Eur. J. Clin. Nutri. 69 (2015) 442-448. https://doi.org/10.1038/ejcn.2014.231.
Crossref Google Scholar
Food Science and Human Wellness
Volume 13 Issue 1,
January 2024
Pages 1-15
DOI: 10.26599/FSHW.2022.9250001
Cite this article:
Duffuler P, Bhullar KS, Wu J. Targeting gut microbiota in osteoporosis: impact of the microbial based functional food ingredients. Food Science and Human Wellness, 2024, 13(1): 1-15. https://doi.org/10.26599/FSHW.2022.9250001

3878

Views

963

Downloads

14

Crossref

15

Web of Science

16

Scopus

0

CSCD

Altmetrics
Received: 28 June 2022
Revised: 12 September 2022
Accepted: 02 October 2022
Published: 01 June 2023
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return