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Bifidobacterium lactis Probio-M8 improves bone metabolism in patients with postmenopausal osteoporosis, possibly by modulating the gut microbiota

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European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Postmenopausal osteoporosis (PMO) is usually managed by conventional drug treatment. However, prolonged use of these drugs cause side effects. Gut microbiota may be a potential target for treatment of PMO. This work was a three-month intervention trial aiming to evaluate the added effect of probiotics as adjunctive treatment for PMO.

Methods

Forty patients with PMO were randomized into probiotic (n = 20; received Bifidobacterium animalis subsp. lactis Probio-M8 [Probio-M8], calcium, calcitriol) and placebo (n = 20; received placebo material, calcium, calcitriol) groups. The bone mineral density of patients was measured at month 0 (0 M; baseline) and month 3 (3 M; after three-month intervention). Blood and fecal samples were collected 0 M and 3 M. Only 15 and 12 patients from Probio-M8 and placebo groups, respectively, provided complete fecal samples for gut microbiota analysis.

Results

No significant change was observed in the bone mineral density of patients at 3 M. Co-administering Probio-M8 improved the bone metabolism, reflected by an increased vitamin D3 level and decreased PTH and procalcitonin levels in serum at 3 M. Fecal metagenomic analysis revealed modest changes in the gut microbiome in both groups at 3 M. Interestingly, Probio-M8 co-administration affected the gut microbial interactive correlation network, particularly the short-chain fatty acid-producing bacteria. Probio-M8 co-administration significantly increased genes encoding some carbohydrate metabolism pathways (including ABC transporters, the phosphotransferase system, and fructose and mannose metabolism) and a choline-phosphate cytidylyltransferase.

Conclusions

Co-administering Probio-M8 with conventional drugs/supplements was more efficacious than conventional drugs/supplements alone in managing PMO. Our study shed insights into the beneficial mechanism of probiotic adjunctive treatment.

Registration number of clinical trial

Chinese Clinical Trial Registry (identifier number: ChiCTR1800019268).

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Data availability

The sequence dataset was deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database (accession number PRJNA773596).

References

  1. Baccaro LF, Conde DM, Costa-Paiva L, Pinto-Neto AM (2015) The epidemiology and management of postmenopausal osteoporosis: a viewpoint from Brazil. Clin Interv Aging 10:583

    Article  PubMed  PubMed Central  Google Scholar 

  2. Noh J-Y, Yang Y, Jung H (2020) Molecular mechanisms and emerging therapeutics for osteoporosis. Int J Mol Sci 21(20):7623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. He J, Xu S, Zhang B, Xiao C, Chen Z, Si F, Fu J, Lin X, Zheng G, Yu G (2020) Gut microbiota and metabolite alterations associated with reduced bone mineral density or bone metabolic indexes in postmenopausal osteoporosis. Aging (Albany NY) 12(9):8583

    Article  CAS  PubMed  Google Scholar 

  4. Rachner TD, Khosla S, Hofbauer LC (2011) Osteoporosis: now and the future. The Lancet 377(9773):1276–1287

    Article  CAS  Google Scholar 

  5. Seely KD, Kotelko CA, Douglas H, Bealer B, Brooks AE (2021) The Human gut microbiota: a key mediator of osteoporosis and osteogenesis. Int J Mol Sci 22(17):9452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ringe JD (2020) Plain vitamin D or active vitamin D in the treatment of osteoporosis: where do we stand today? Arch Osteoporos 15(1):182. https://doi.org/10.1007/s11657-020-00842-0

    Article  PubMed  Google Scholar 

  7. Tilyard MW, Spears GFS, Thomson J, Dovey S (1992) Treatment of postmenopausal osteoporosis with calcitriol or calcium. N Engl J Med 326(6):357–362. https://doi.org/10.1056/nejm199202063260601

    Article  CAS  PubMed  Google Scholar 

  8. Janoušek J, Pilařová V, Macáková K, Nomura A, Veiga-Matos J, Silva DDD, Remião F, Saso L, Malá-Ládová K, Malý J, Nováková L, Mladěnka P (2022) Vitamin D: sources, physiological role, biokinetics, deficiency, therapeutic use, toxicity, and overview of analytical methods for detection of vitamin D and its metabolites. Criti rev clin lab sci. https://doi.org/10.1080/10408363.2022.2070595

    Article  Google Scholar 

  9. Rizzoli R, Biver E (2020) Are probiotics the new calcium and vitamin D for bone health? Curr Osteoporos Rep 18(3):273–284

    Article  PubMed  Google Scholar 

  10. Ling C-w, Miao Z, Xiao M-l, Zhou H, Jiang Z, Fu Y, Xiong F, L-s-y Z, Liu Y-p, Wu Y-y (2021) The association of gut microbiota with osteoporosis is mediated by amino acid metabolism: multiomics in a large cohort. J Clin Endocrinol Metab 106(10):e3852–e3864

    Article  PubMed  Google Scholar 

  11. Shen Q, Zhang C, Qin X, Zhang H, Zhang Z, Richel A (2021) Modulation of gut microbiota by chondroitin sulfate calcium complex during alleviation of osteoporosis in ovariectomized rats. Carbohyd Polym 266:118099

    Article  CAS  Google Scholar 

  12. Das M, Cronin O, Keohane DM, Cormac EM, Nugent H, Nugent M, Molloy C, O’Toole PW, Shanahan F, Molloy MG (2019) Gut microbiota alterations associated with reduced bone mineral density in older adults. Rheumatology 58(12):2295–2304

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) 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):506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  14. Jia L, Tu Y, Jia X, Du Q, Zheng X, Yuan Q, Zheng L, Zhou X, Xu X (2021) Probiotics ameliorate alveolar bone loss by regulating gut microbiota. Cell Prolif 54(7):e13075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Montazeri-Najafabady N, Ghasemi Y, Dabbaghmanesh MH, Talezadeh P, Koohpeyma F, Gholami A (2019) Supportive role of probiotic strains in protecting rats from ovariectomy-induced cortical bone loss. Probiotics antimicrob proteins 11(4):1145–1154

    Article  CAS  PubMed  Google Scholar 

  16. Jafarnejad S, Djafarian K, Fazeli MR, Yekaninejad MS, Rostamian A, Keshavarz SA (2017) Effects of a multispecies probiotic supplement on bone health in osteopenic postmenopausal women: a randomized, double-blind, controlled trial. J Am Coll Nutr 36(7):497–506

    Article  CAS  PubMed  Google Scholar 

  17. Takimoto T, Hatanaka M, Hoshino T, Takara T, Tanaka K, Shimizu A, Morita H, Nakamura T (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. https://doi.org/10.12938/bmfh.18-006

    Article  PubMed  PubMed Central  Google Scholar 

  18. Jansson P-A, Curiac D, Ahrén IL, Hansson F, Niskanen TM, Sjögren K, Ohlsson C (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. Lancet Rheumatol 1(3):e154–e162

    Article  Google Scholar 

  19. Nilsson A, Sundh D, Bäckhed F, Lorentzon M (2018) 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(3):307–317

    Article  CAS  PubMed  Google Scholar 

  20. Billington EO, Mahajan A, Benham JL, Raman M (2021) Effects of probiotics on bone mineral density and bone turnover: a systematic review. Crit Rev Food Sci Nutr. https://doi.org/10.1080/10408398.2021.1998760

    Article  PubMed  Google Scholar 

  21. Zhang W, Wang Y, Li K, Kwok L-Y, Liu W, Zhang H (2020) Modulation of fatty acid metabolism improves oxygen tolerance of Bifidobacterium animalis ssp lactis Probio-M8. J Dairy Sci 103(10):8791–8795

    Article  CAS  PubMed  Google Scholar 

  22. Sun H, Zhao F, Liu Y, Ma T, Jin H, Quan K, Leng B, Zhao J, Yuan X, Li Z, Li F, Kwok L-Y, Zhang S, Sun Z, Zhang J, Zhang H (2022) Probiotics synergized with conventional regimen in managing Parkinson’s disease. npj Parkinson’s Disease. https://doi.org/10.1038/s41531-022-00327-6

    Article  PubMed  PubMed Central  Google Scholar 

  23. Liu A, Ma T, Xu N, Jin H, Zhao F, Kwok L-Y, Zhang H, Zhang S, Sun Z (2021) Adjunctive probiotics alleviates asthmatic symptoms via modulating the gut microbiome and serum metabolome. Microbiol spectr 9(2):e00859-e1821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Narva M, Nevala R, Poussa T, Korpela R (2004) The effect of Lactobacillus helveticus fermented milk on acute changes in calcium metabolism in postmenopausal women. Eur J Nutr 43(2):61–68. https://doi.org/10.1007/s00394-004-0441-y

    Article  CAS  PubMed  Google Scholar 

  25. Dinan TG, Stanton C, Cryan JF (2013) Psychobiotics: a novel class of psychotropic. Biol Psychiat 74(10):720–726

    Article  CAS  PubMed  Google Scholar 

  26. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kang DD, Li F, Kirton E, Thomas A, Egan R, An H, Wang Z (2019) MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 7:e7359

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lee J, Jang JY, Kwon MS, Lim SK, Kim N, Lee J, Park HK, Yun M, Shin MY, Jo HE, Oh YJ, Ryu BH, Ko MY, Joo W, Choi HJ (2018) Mixture of two lactobacillus plantarum strains modulates the gut microbiota structure and regulatory t cell response in diet-induced obese mice. Mol Nutr Food Res 62(24):11. https://doi.org/10.1002/mnfr.201800329

    Article  CAS  Google Scholar 

  29. Vasimuddin M, Misra S, Li H, Aluru S (2019) Efficient architecture-aware acceleration of BWA-MEM for multicore systems. 2019 IEEE International Parallel and Distributed Processing Symposium (IPDPS). Piscataway, IEEE, pp 314–324

    Google Scholar 

  30. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  31. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25(7):1043–1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Olm MR, Brown CT, Brooks B, Banfield JF (2017) dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J 11(12):2864–2868. https://doi.org/10.1038/ismej.2017.126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wood DE, Lu J, Langmead B (2019) Improved metagenomic analysis with Kraken 2. Genome Biol 20(1):1–13

    Article  Google Scholar 

  34. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11(1):1–11

    Article  Google Scholar 

  35. Becker KL, Snider R, Nylen ES (2010) Procalcitonin in sepsis and systemic inflammation: a harmful biomarker and a therapeutic target. Br J Pharmacol 159(2):253–264. https://doi.org/10.1111/j.1476-5381.2009.00433.x

    Article  CAS  PubMed  Google Scholar 

  36. Yerlikaya FH, Onmaz DE (2022) Inflammation and Bone turnover markers in adult obesity. J Clin Densitom. https://doi.org/10.1016/j.jocd.2022.08.002

    Article  PubMed  Google Scholar 

  37. Kärkkäinen MU, Lamberg-Allardt CJ, Ahonen S, Välimäki M (2001) Does it make a difference how and when you take your calcium? The acute effects of calcium on calcium and bone metabolism. Am J Clin Nutr 74(3):335–342

    Article  PubMed  Google Scholar 

  38. Narva M, Collin M, Lamberg-Allardt C, Kärkkäinen M, Poussa T, Vapaatalo H, Korpela R (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(4):228–234

    Article  CAS  PubMed  Google Scholar 

  39. Bell TD, Demay MB, Burnett-Bowie SAM (2010) The biology and pathology of vitamin D control in bone. J Cell Biochem 111(1):7–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Holick MF (2007) Vitamin D deficiency. N Engl J Med 357(3):266–281

    Article  CAS  PubMed  Google Scholar 

  41. Heaney RP, Dowell MS, Hale CA, Bendich A (2003) Calcium absorption varies within the reference range for serum 25-hydroxyvitamin D. J Am Coll Nutr 22(2):142–146

    Article  CAS  PubMed  Google Scholar 

  42. Zaidi M, Moonga BS, Abe E (2002) Calcitonin and bone formation: a knockout full of surprises. J Clin Investig 110(12):1769–1771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Davey RA, Findlay DM (2013) Calcitonin: physiology or fantasy? J Bone Miner Res 28(5):973–979

    Article  CAS  PubMed  Google Scholar 

  44. Li J, Qiao H, LIN T, (2021) Diagnostic value of serum procalcitonin level combined with quantitative CT in elderly women with painful osteoporosis and its correlation with disease severity. Chin J Endocr Surg 6:189–192

    Google Scholar 

  45. MacDonald IJ, Tsai H-C, Chang A-C, Huang C-C, Yang S-F, Tang C-H (2021) Melatonin Inhibits osteoclastogenesis and osteolytic bone metastasis: implications for osteoporosis. Int J Mol Sci 22(17):9435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Kuo T-R, Chen C-H (2017) Bone biomarker for the clinical assessment of osteoporosis: recent developments and future perspectives. Biomark res 5(1):1–9

    Article  Google Scholar 

  47. Britton RA, Irwin R, Quach D, Schaefer L, Zhang J, Lee T, Parameswaran N, McCabe LR (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J cell physiol 229(11):1822–1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Parvaneh K, Ebrahimi M, Sabran MR, Karimi G, Hwei ANM, Abdul-Majeed S, Ahmad Z, Ibrahim Z, Jamaluddin R (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 2015:10. https://doi.org/10.1155/2015/897639

    Article  CAS  Google Scholar 

  49. Singer FR, Eyre DR (2008) Using biochemical markers of bone turnover in clinical practice. Clevel Clin J Med 75(10):739–750

    Article  Google Scholar 

  50. Liu ZY, Chen RQ, Jiang YT, Yang Y, He L, Luo CX, Dong JW, Rong LM (2019) A meta-analysis of serum osteocalcin level in postmenopausal osteoporotic women compared to controls. BMC Musculoskelet Disord 20(1):7. https://doi.org/10.1186/s12891-019-2863-y

    Article  CAS  Google Scholar 

  51. Rettedal EA, Ilesanmi-Oyelere BL, Roy NC, Coad J, Kruger MC (2021) The gut microbiome is altered in postmenopausal women with osteoporosis and osteopenia. JBMR plus 5(3):e10452. https://doi.org/10.1002/jbm4.10452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sun B, Ma T, Li Y, Yang N, Li B, Zhou X, Guo S, Zhang S, Kwok L-Y, Sun Z, Zhang H (2022) Bifidobacterium lactis probio-M8 adjuvant treatment confers added benefits to patients with coronary artery disease via target modulation of the gut-heart/-brain axes. Msystems. https://doi.org/10.1128/msystems.00100-22

    Article  PubMed  PubMed Central  Google Scholar 

  53. Liu A, Ma T, Xu N, Jin H, Zhao F, Kwok L-Y, Zhang H, Zhang S, Sun Z (2021) Adjunctive probiotics alleviates asthmatic symptoms via modulating the gut microbiome and serum metabolome. Microbio spectr. https://doi.org/10.1128/Spectrum.00859-21

    Article  Google Scholar 

  54. Xu HY, Ma C, Zhao FY, Chen P, Liu YH, Sun ZH, Cui LH, Kwok LY, Zhang HP (2021) Adjunctive treatment with probiotics partially alleviates symptoms and reduces inflammation in patients with irritable bowel syndrome. Eur J Nutr 60(5):2553–2565. https://doi.org/10.1007/s00394-020-02437-4

    Article  CAS  PubMed  Google Scholar 

  55. Shanahan F, Hill C (2019) Language, numeracy and logic in microbiome science. Nat Rev Gastroenterol Hepatol 16(7):387–388. https://doi.org/10.1038/s41575-019-0163-5

    Article  PubMed  Google Scholar 

  56. Matchado MS, Lauber M, Reitmeier S, Kacprowski T, Baumbach J, Haller D, List M (2021) Network analysis methods for studying microbial communities: a mini review. Comput Struct Biotechnol J 19:2687–2698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Zhao L, Zhang F, Ding X, Wu G, Lam YY, Wang X, Fu H, Xue X, Lu C, Ma J (2018) Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science 359(6380):1151–1156

    Article  CAS  PubMed  Google Scholar 

  58. Coker OO, Nakatsu G, Dai RZ, Wu WKK, Wong SH, Ng SC, Chan FKL, Sung JJY, Yu J (2019) Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut 68(4):654–662

    Article  CAS  PubMed  Google Scholar 

  59. Xu H, Zhao F, Hou Q, Huang W, Liu Y, Zhang H, Sun Z (2019) Metagenomic analysis revealed beneficial effects of probiotics in improving the composition and function of the gut microbiota in dogs with diarrhoea. Food Funct 10(5):2618–2629

    Article  CAS  PubMed  Google Scholar 

  60. Kelder T, Stroeve JHM, Bijlsma S, Radonjic M, Roeselers G (2014) Correlation network analysis reveals relationships between diet-induced changes in human gut microbiota and metabolic health. Nutr Diabetes 4(6):e122–e122. https://doi.org/10.1038/nutd.2014.18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Ling CW, Miao ZL, Xiao ML, Zhou HW, Jiang ZL, Fu YQ, Xiong F, Zuo LSY, Liu YP, Wu YY, Jing LP, Dong HL, Chen GD, Ding D, Wang C, Zeng FF, Zhu HL, He Y, Zheng JS, Chen YM (2021) The association of gut microbiota with osteoporosis is mediated by amino acid metabolism: multiomics in a large cohort. J Clin Endocrinol Metab 106(10):E3852–E3864. https://doi.org/10.1210/clinem/dgab492

    Article  PubMed  Google Scholar 

  62. Hayes CA, Dalia TN, Dalia AB (2017) Systematic genetic dissection of PTS in Vibrio cholerae uncovers a novel glucose transporter and a limited role for PTS during infection of a mammalian host. Mol Microbiol 104(4):568–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Koropatkin NM, Cameron EA, Martens EC (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10(5):323–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Morishita, (2009) Fluvastatin improves osteoporosis in fructose-fed insulin resistant model rats through blockade of the classical mevalonate pathway and antioxidant action. Int J Mol Med. https://doi.org/10.3892/ijmm_00000167

    Article  PubMed  Google Scholar 

  65. Mei ZD, Dong X, Qian Y, Hong D, Xie ZA, Yao GF, Qin A, Gao SY, Hu JY, Liang LM, Zheng Y, Su JC (2020) Association between the metabolome and bone mineral density in a Chinese population. EBioMedicine 62:10. https://doi.org/10.1016/j.ebiom.2020.103111

    Article  CAS  Google Scholar 

  66. Farina EK, Kiel DP, Roubenoff R, Schaefer EJ, Cupples LA, Tucker KL (2012) Plasma phosphatidylcholine concentrations of polyunsaturated fatty acids are differentially associated with hip bone mineral density and hip fracture in older adults: The framingham osteoporosis study. J Bone Miner Res 27(5):1222–1230. https://doi.org/10.1002/jbmr.1581

    Article  CAS  PubMed  Google Scholar 

  67. Aleidi SM, Alnehmi EA, Alshaker M, Masood A, Benabdelkamel H, Al-Ansari MM, Rahman AMA (2021) A distinctive human metabolomics alteration associated with osteopenic and osteoporotic patients. Metabolites 11(9):14. https://doi.org/10.3390/metabo11090628

    Article  CAS  Google Scholar 

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Funding

This research was supported by Inner Mongolia Science and Technology Major Projects (2021ZD0014) and the Earmarked Fund for CARS-36.

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  1. Feiyan Zhao and Zhenguo Guo are equally contributed to this work.

Authors and Affiliations

  1. Inner Mongolia Key Laboratory of Dairy Biotechnology and Engineering, Key Laboratory of Dairy Products Processing, Ministry of Agriculture and Rural Affairs, Key Laboratory of Dairy Biotechnology and Engineering, Ministry of Education, Inner Mongolia Agricultural University, Hohhot, 010018, Inner Mongolia, China

    Feiyan Zhao, Lai-Yu Kwok, Zhixin Zhao, Kexin Wang, Yalin Li, Zhihong Sun & Heping Zhang

  2. Department of Orthopaedics, The Affiliated Hospital of Inner Mongolia Medical University, Hohhot, 010018, Inner Mongolia, China

    Zhenguo Guo & Jianmin Zhao

  3. Department of Hand and Foot Surgery, Huizhou Central People’s Hospital, Huizhou, 516001, Guangdong, China

    Zhenguo Guo

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Contributions

JZ and HZ conceived and designed the trial. ZS supervised all bench work. ZG recruited patients, collected and summarized data. FZ, ZZ, KW, and YL analyzed the metagenomic sequencing data. FZ wrote the manuscript. LY Kwok reviewed and revised the manuscript critically. All authors discussed the results and commented on the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jianmin Zhao or Heping Zhang.

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Conflict of interest

The authors declare no competing interests.

Ethical approval and consent to participate

This intervention trial was approved by Ethics Committee of the Affiliated Hospital of Inner Mongolia Medical University (project number KY 2018010) and registered in the Chinese Clinical Trial Registry (http://www.chictr.org.cn/; identifier number: ChiCTR1800019268). An informed consent was signed by all subjects prior to the study.

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Zhao, F., Guo, Z., Kwok, LY. et al. Bifidobacterium lactis Probio-M8 improves bone metabolism in patients with postmenopausal osteoporosis, possibly by modulating the gut microbiota. Eur J Nutr 62, 965–976 (2023). https://doi.org/10.1007/s00394-022-03042-3

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