Abstract
Objectives
Osteoporosis is characterized by slow deterioration in bone mass and disruption of its structure, leading to an increased risk of bone fractures. Gut microbiota plays an important role in the transport and absorption of nutrients needed for bone health. Akkermansia muciniphila is one of the gut microbiota members that its beneficial role in prevention of metabolic disorder was suggested. The aim of the current pilot study was the assessment of fecal A. muciniphila in patients with osteoporosis and osteopenia.
Methods
A total of 36 subjects including eight with osteoporosis (three men and five women), eight with osteopenia (two men and six women), and 20 normal controls (six men and 14 women) were selected. Microbial genome was extracted from fresh stool samples. The bacterial load was determined by quantitative real-time PCR using 16S rRNA specific primers.
Results
The participants’ mean age in the osteoporosis, osteopenia and control groups were 61.71, 45 and 45.05 years, respectively. The majority of osteoporosis patients were post-menopause women, while in osteopenia group was pre-menopause. There were significant differences in terms of age, T-score, Z-score, and menopause among groups (P value < 0.05). The presence of A. muciniphila was higher in the healthy group compared to osteopenia group; however, these differences were not statistically significant.
Conclusions
In conclusion, however, there was no statistically significant difference between the study groups; it seems that the load of A. muciniphila may be related to bone health. Further in vivo and in vitro studies are needed to investigate the immunological and biochemical pathways.
Similar content being viewed by others
Data availability
Not applicable.
References
Ohlsson C, Sjögren K. Effects of the gut microbiota on bone mass. Trends Endocrinol Metab. 2015;26(2):69–74.
Kim B-J, Koh J-M. Coupling factors involved in preserving bone balance. Cell Mol Life Sci. 2019;76(7):1243–53.
Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci. 2004;101(44):15718–23.
Behera J, Ison J, Tyagi SC, Tyagi N. The role of gut microbiota in bone homeostasis. Bone. 2020;135:115317. https://doi.org/10.1016/j.bone.2020.115317.
Gomaa EZ. Human gut microbiota/microbiome in health and diseases: a review. Antonie Van Leeuwenhoek. 2020;113:2019–40. https://doi.org/10.1007/s10482-020-01474-7.
Weaver CM. Diet, gut microbiome, and bone health. Curr Osteoporos Rep. 2015;13(2):125–30.
Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol. 2007;73(23):7767–70.
Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. Nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 2004;54(5):1469–76.
Ottman N, Geerlings SY, Aalvink S, de Vos WM, Belzer C. Action and function of Akkermansia muciniphila in microbiome ecology, health and disease. Best Pract Res Clin Gastroenterol. 2017;31(6):637–42.
Tu P, Bian X, Chi L, Gao B, Ru H, Knobloch TJ, et al. Characterization of the functional changes in mouse gut microbiome associated with increased Akkermansia muciniphila population modulated by dietary black raspberries. ACS omega. 2018;3(9):10927–37.
Depommier C, Everard A, Druart C, Plovier H, Van Hul M, Vieira-Silva S, et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nat Med. 2019;25(7):1096–103.
Zhang T, Li Q, Cheng L, Buch H, Zhang F. Akkermansia muciniphila is a promising probiotic. Microb Biotechnol. 2019;12(6):1109–25.
Ashrafian F, Shahryari A, Behrouzi A, Moradi HR, Lari A, Hadifar S, et al. Akkermansia muciniphila-derived extracellular vesicles as a mucosal delivery vector for amelioration of obesity in mice. Front Microbiol. 2019;10:2155.
David Yatsonsky I, Pan K, Shendge VB, Liu J, Ebraheim NA. Linkage of microbiota and osteoporosis: a mini literature review. World J Orthop. 2019;10(3):123.
Schneeberger M, Everard A, Gómez-Valadés AG, Matamoros S, Ramírez S, Delzenne NM, et al. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep. 2015;5:16643.
Compston JE, McClung MR, Leslie WD. Osteoporosis. Lancet. 2019;393(10169):364–76.
Ejtahed H-S, Hoseini-Tavassol Z, Khatami S, Zangeneh M, Behrouzi A, Badi SA, et al. Main gut bacterial composition differs between patients with type 1 and type 2 diabetes and non-diabetic adults. J Diabetes Metab Disord. 2020;19(1):265–71.
De Martinis M, Sirufo MM, Ginaldi L. Osteoporosis: Current and emerging therapies targeted to immunological checkpoints. Curr Med Chem. 2020;27(37):6356–72.
Locantore P, Del Gatto V, Gelli S, Paragliola RM, Pontecorvi A. The interplay between immune system and microbiota in osteoporosis. Mediat Inflamm. 2020;2020:1–8.
Wang J, Wang Y, Gao W, Wang B, Zhao H, Zeng Y, et al. Diversity analysis of gut microbiota in osteoporosis and osteopenia patients. PeerJ. 2017;5:e3450.
Das M, Cronin O, Keohane DM, Cormac EM, Nugent H, Nugent M, et al. Gut microbiota alterations associated with reduced bone mineral density in older adults. Rheumatology. 2019;58(12):2295–304.
Rizzoli, R. Nutritional influence on bone: role of gut microbiota. Aging Clin Exp Res. 2019;31:743–51. https://doi.org/10.1007/s40520-019-01131-8.
McCabe LR, Parameswaran N. Understanding the gut-bone signaling Axis: mechanisms and therapeutic implications. Berlin: Springer; 2017.
Quach D, Britton RA. Gut microbiota and bone health. In: Understanding the Gut-Bone Signaling Axis. Berlin: Springer; 2017. p. 47–58.
Salehi I, Khazaeli S, Najafizadeh SR, Ashraf H, Malekpour M. High prevalence of low bone density in young Iranian healthy individuals. Clin Rheumatol. 2009;28(2):173–7.
Khan A, Fortier M, Reid R, Abramson BL, Blake J, Desindes S, et al. Osteoporosis in menopause. J Obstet Gynaecol Can. 2014;36(9):839–40.
Hsu T-L, Tantoh DM, Chou Y-H, Hsu S-Y, Ho C-C, Lung C-C, et al. Association between osteoporosis and menopause in relation to SOX6 rs297325 variant in Taiwanese women. Menopause. 2020;27(8):887.
Society NAM. Management of osteoporosis in postmenopausal women: 2006 position statement of The North American Menopause Society. Menopause. 2006;13(3):340.
Sjögren K, Engdahl C, Henning P, Lerner UH, Tremaroli V, Lagerquist MK, et al. The gut microbiota regulates bone mass in mice. J Bone Miner Res. 2012;27(6):1357–67.
McCabe L, Britton RA, Parameswaran N. Prebiotic and probiotic regulation of bone health: role of the intestine and its microbiome. Curr Osteoporos Rep. 2015;13(6):363–71.
Ibáñez L, Rouleau M, Wakkach A, Blin-Wakkach C. Gut microbiome and bone. Joint Bone Spine. 2019;86(1):43–7.
Pazzini CA, Pereira LJ, da Silva TA, Montalvany-Antonucci CC, Macari S, Marques LS, et al. Probiotic consumption decreases the number of osteoclasts during orthodontic movement in mice. Arch Oral Biol. 2017;79:30–4.
Li J-Y, Chassaing B, Tyagi AM, Vaccaro C, Luo T, Adams J, et al. Sex steroid deficiency–associated bone loss is microbiota dependent and prevented by probiotics. J Clin Invest. 2016;126(6):2049–63.
Liu J-H, Yue T, Luo Z-W, Cao J, Yan Z-Q, Jin L, et al. Akkermansia Muciniphila promotes bone fracture healing by enhancing Preosteoclast-associated type H vessel formation. 2019. https://doi.org/10.2139/ssrn.3405551.
Acknowledgments
We thank all the lab members of Microbiology Research Center (MRC) & Department of Biochemistry, Pasteur Institute of Iran, and Amir al-Momenin Hospital for their assistance in this project.
Funding
This project was funded by the Research Committee of Pasteur Institute of Iran (No. 1058/1061). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Contributions
SK performed the experiments, sampling, DNA extraction, and real-time PCR, analyzed the data, and wrote the paper, prepared figures and Tables. MA, ZHT, and AK; sampling, sample preparation and DNA extraction. SS; serum preparation and biochemical test. SDS, SK, and MZ; conceived and designed the experiments, reviewed drafts of the paper. HE, FA and ZHT; reviewed and edited the drafts of paper.
Corresponding author
Ethics declarations
Conflict of interest
No relevant conflict of interest has been declared by the authors.
Ethics approval
The following information was supplied relating to ethical approvals (i.e., approving body reference numbers (No. 1284) Pasteur Institute of Iran, Biomedical research ethics committee.
Code availability
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Keshavarz Azizi Raftar, S., Hoseini Tavassol, Z., Amiri, M. et al. Assessment of fecal Akkermansia muciniphila in patients with osteoporosis and osteopenia: a pilot study. J Diabetes Metab Disord 20, 279–284 (2021). https://doi.org/10.1007/s40200-021-00742-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40200-021-00742-1