Skip to main content

Advertisement

SpringerLink
Log in

Changes in the fecal microbiota of breast cancer patients based on 16S rRNA gene sequencing: a systematic review and meta-analysis

  • RESEARCH ARTICLE
  • Published:
Clinical and Translational Oncology Aims and scope Submit manuscript

Abstract

Purpose

Breast cancer (BC) is a devastating disease for women. Microbial influences may be involved in the development and progression of breast cancer. This study aimed to investigate the difference in intestinal flora abundance between breast cancer patients and healthy controls (HC) based on previous 16S ribosomal RNA (rRNA) gene sequencing results, which have been scattered and inconsistent in previous studies.

Materials and methods

In agreement with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA), we searched for pertinent literature in Pubmed, Embase, Cochrane Library, and Web of Science databases from build until February 1, 2023. Relative abundance, diversity of intestinal microflora by level, microbial composition, community structure, diversity index, and other related data were extracted. We used a fixed or random effects model for data analysis. We also conducted funnel plot analysis, sensitivity analysis, Egger's, and Begg’s tests to assess the bias risk.

Results

A total of ten studies involving 734 BC patients were enrolled. It was pointed out that there were significant differences in the Chao index between BC and HC in these studies [SMD = − 175.44 (95% CI − 246.50 to − 104.39)]. The relative abundance of Prevotellaceae [SMD = − 0.27 (95% CI − 0.39 to − 0.15)] and Bacteroides [SMD = 0.36 (95% CI 0.23–0.49)] was significantly different. In the included articles, the relative abundance of Prevotellaceae, Ruminococcus, Roseburia inulinivorans, and Faecalibacterium prausnitzii decreased in BC. Accordingly, the relative richness of Erysipelotrichaceae was high in BC.

Conclusions

This observational meta-analysis revealed that the changes in gut microbiota were correlated with BC, and the changes in some primary fecal microbiota might affect the beginning of breast cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Availability of data and material

Not applicable.

References

  1. Akram M, Iqbal M, Daniyal M, Khan AU. Awareness and current knowledge of breast cancer. Biol Res. 2017;50(1):33.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Trapani D, Ginsburg O, Fadelu T, Lin NU, Hassett M, Ilbawi AM, et al. Global challenges and policy solutions in breast cancer control. Cancer Treat Rev. 2022;104:102339.

    Article  PubMed  Google Scholar 

  3. Ginsburg O, Bray F, Coleman MP, Vanderpuye V, Eniu A, Kotha SR, et al. The global burden of women’s cancers: a grand challenge in global health. Lancet. 2017;389(10071):847–60.

    Article  PubMed  Google Scholar 

  4. Lei S, Zheng R, Zhang S, Wang S, Chen R, Sun K, et al. Global patterns of breast cancer incidence and mortality: a population-based cancer registry data analysis from 2000 to 2020. Cancer Commun (Lond). 2021;41(11):1183–94.

    Article  PubMed  Google Scholar 

  5. Gray JM, Rasanayagam S, Engel C, Rizzo J. State of the evidence 2017: an update on the connection between breast cancer and the environment. Environ Health. 2017;16(1):94.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Sun Y-S, Zhao Z, Yang Z-N, Xu F, Lu H-J, Zhu Z-Y, et al. Risk factors and preventions of breast cancer. Int J Biol Sci. 2017;13(11):1387–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Plottel CS, Blaser MJ. Microbiome and malignancy. Cell Host Microbe. 2011;10(4):324–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Siddiqui R, Makhlouf Z, Alharbi AM, Alfahemi H, Khan NA. The gut microbiome and female health. Biology (Basel). 2022;11(11):1683.

    CAS  PubMed  Google Scholar 

  9. Lasagna A, Zuccaro V, Ferraris E, Corbella M, Bruno R, Pedrazzoli P. Covid-19 and breast cancer: may the microbiome be the issue? Future Oncol. 2021;17(2):123–6.

    Article  CAS  PubMed  Google Scholar 

  10. Fernández MF, Reina-Pérez I, Astorga JM, Rodríguez-Carrillo A, Plaza-Díaz J, Fontana L. Breast cancer and its relationship with the microbiota. Int J Environ Res Public Health. 2018;15(8):1747.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Laborda-Illanes A, Sanchez-Alcoholado L, Dominguez-Recio ME, Jimenez-Rodriguez B, Lavado R, Comino-Méndez I, et al. Breast and gut microbiota action mechanisms in breast cancer pathogenesis and treatment. Cancers. 2020;12(9):2465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Komorowski AS, Pezo RC. Untapped “-omics”: the microbial metagenome, estrobolome, and their influence on the development of breast cancer and response to treatment. Breast Cancer Res Treat. 2020;179(2):287–300.

    Article  CAS  PubMed  Google Scholar 

  13. Goedert JJ, Hua X, Bielecka A, Okayasu I, Milne GL, Jones GS, et al. Postmenopausal breast cancer and oestrogen associations with the IgA-coated and IgA-noncoated faecal microbiota. Br J Cancer. 2018;118(4):471–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Jackson MA, Verdi S, Maxan M-E, Shin CM, Zierer J, Bowyer RCE, et al. Gut microbiota associations with common diseases and prescription medications in a population-based cohort. Nat Commun. 2018;9(1):2655.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Zhu J, Liao M, Yao Z, Liang W, Li Q, Liu J, et al. Breast cancer in postmenopausal women is associated with an altered gut metagenome. Microbiome. 2018;6(1):136.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Watts GS, Youens-Clark K, Slepian MJ, Wolk DM, Oshiro MM, Metzger GS, et al. 16s rrna gene sequencing on a benchtop sequencer: accuracy for identification of clinically important bacteria. J Appl Microbiol. 2017;123(6):1584–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Gao B, Chi L, Zhu Y, Shi X, Tu P, Li B, et al. An introduction to next generation sequencing bioinformatic analysis in gut microbiome studies. Biomolecules. 2021;11(4):961–8.

    Article  Google Scholar 

  18. Aarnoutse R, Hillege LE, Ziemons J, De Vos-Geelen J, de Boer M, Aerts E, et al. Intestinal microbiota in postmenopausal breast cancer patients and controls. Cancers. 2021;13(24):6200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Goedert JJ, Jones G, Hua X, Xu X, Yu G, Flores R, et al. Investigation of the association between the fecal microbiota and breast cancer in postmenopausal women: a population-based case-control pilot study. J Natl Cancer Inst. 2015;107(8):djv147

  20. Shrode RL, Knobbe JE, Cady N, Yadav M, Hoang J, Cherwin C, et al. Breast cancer patients from the midwest region of the united states have reduced levels of short-chain fatty acid-producing gut bacteria. Sci Rep. 2023;13(1):526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Caleça T, Ribeiro P, Vitorino M, Menezes M, Sampaio-Alves M, Mendes AD, et al. Breast cancer survivors and healthy women: could gut microbiota make a difference?-“biotacancersurvivors”: a case–control study. Cancers. 2023;15(3):594.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Atkins D, Fink K, Slutsky J. Better information for better health care: the evidence-based practice center program and the agency for healthcare research and quality. Ann Intern Med. 2005;142(12 Pt 2):1035–41.

    Article  PubMed  Google Scholar 

  24. Bobin-Dubigeon C, Luu HT, Leuillet S, Lavergne SN, Carton T, Le Vacon F, et al. Faecal microbiota composition varies between patients with breast cancer and healthy women: a comparative case-control study. Nutrients. 2021;13(8):2705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Byrd DA, Vogtmann E, Wu Z, Han Y, Wan Y, Clegg-Lamptey JN, et al. Associations of fecal microbial profiles with breast cancer and nonmalignant breast disease in the Ghana Breast Health Study. Int J Cancer. 2021;148(11):2712–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. He C, Liu Y, Ye SD, Yin SW, Gu JF. Changes of intestinal microflora of breast cancer in premenopausal women. Eur J Clin Microbiol Infect Dis. 2021;40(3):503–13.

    Article  CAS  PubMed  Google Scholar 

  27. Ma Z, Qu M, Wang X. Analysis of gut microbiota in patients with breast cancer and benign breast lesions. Pol J Microbiol. 2022;71(2):217–26.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Wenhui Y, Zhongyu X, Kai C, Zhaopeng C, Jinteng L, Mengjun M, et al. Variations in the gut microbiota in breast cancer occurrence and bone metastasis. Front Microbiol. 2022;13:894283.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Whittaker RH, Damschen EI, Harrison S. Plant community data collected by Robert H. Whittaker in the Siskiyou Mountains, Oregon and California, USA. Ecology. 2022;103(9):e3764.

    Article  PubMed  Google Scholar 

  30. Sonnenburg JL, Bäckhed F. Diet–microbiota interactions as moderators of human metabolism. Nature. 2016;535(7610):56–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Thu MS, Chotirosniramit K, Nopsopon T, Hirankarn N, Pongpirul K. Human gut, breast, and oral microbiome in breast cancer: a systematic review and meta-analysis. Front Oncol. 2023;13:1144021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Di Modica M, Gargari G, Regondi V, Bonizzi A, Arioli S, Belmonte B, et al. Gut microbiota condition the therapeutic efficacy of trastuzumab in HER2-positive breast cancer. Can Res. 2021;81(8):2195–206.

    Article  Google Scholar 

  33. Terrisse S, Derosa L, Iebba V, Ghiringhelli F, Vaz-Luis I, Kroemer G, et al. Intestinal microbiota influences clinical outcome and side effects of early breast cancer treatment. Cell Death Differ. 2021;28(9):2778–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wang H, Altemus J, Niazi F, Green H, Calhoun BC, Sturgis C, et al. Breast tissue, oral and urinary microbiomes in breast cancer. Oncotarget. 2017;8(50):88122–38.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Garrett WS. Cancer and the microbiota. Science. 2015;348(6230):80–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Mirzaei R, Afaghi A, Babakhani S, Sohrabi MR, Hosseini-Fard SR, Babolhavaeji K, et al. Role of microbiota-derived short-chain fatty acids in cancer development and prevention. Biomed Pharmacother. 2021;139:111619.

    Article  CAS  PubMed  Google Scholar 

  37. González-Bosch C, Boorman E, Zunszain PA, Mann GE. Short-chain fatty acids as modulators of redox signaling in health and disease. Redox Biol. 2021;47:102165.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Cong J, Zhou P, Zhang R. Intestinal microbiota-derived short chain fatty acids in host health and disease. Nutrients. 2022;14(9):1977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. He J, Zhang P, Shen L, Niu L, Tan Y, Chen L, et al. Short-chain fatty acids and their association with signalling pathways in inflammation, glucose and lipid metabolism. Int J Mol Sci. 2020;21(17):6356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Portincasa P, Bonfrate L, Vacca M, De Angelis M, Farella I, Lanza E, et al. Gut microbiota and short chain fatty acids: implications in glucose homeostasis. Int J Mol Sci. 2022;23(3):1105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Xie Q-S, Zhang J-X, Liu M, Liu P-H, Wang Z-J, Zhu L, et al. Short-chain fatty acids exert opposite effects on the expression and function of p-glycoprotein and breast cancer resistance protein in rat intestine. Acta Pharmacol Sin. 2021;42(3):470–81.

    Article  CAS  PubMed  Google Scholar 

  42. Lennicke C, Cochemé HM. Redox metabolism: ROS as specific molecular regulators of cell signaling and function. Mol Cell. 2021;81(18):3691–707.

    Article  CAS  PubMed  Google Scholar 

  43. González-Bosch C, Zunszain PA, Mann GE. Control of redox homeostasis by short-chain fatty acids: implications for the prevention and treatment of breast cancer. Pathogens. 2023;12(3):486.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Dieleman S, Aarnoutse R, Ziemons J, Kooreman L, Boleij A, Smidt M. Exploring the potential of breast microbiota as biomarker for breast cancer and therapeutic response. Am J Pathol. 2021;191(6):968–82.

    Article  CAS  PubMed  Google Scholar 

  45. Parida S, Sharma D. The microbiome–estrogen connection and breast cancer risk. Cells. 2019;8(12):1642.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The National Natural Science Foundations of China provided support for this article (Grant nos. 82060543 and 82060538).

Author information

Author notes

  1. B. Q. Luan and F. Ge contributed equally to this work.

Authors and Affiliations

  1. Department of Breast Surgery, First Affiliated Hospital, Kunming Medical University, Kunming, China

    Biqing Luan, Fei Ge, Xingjia Lu, Zhiqiang Li, Hong Zhang, Jingxuan Wu, Qizhi Yang, Liang Chen & Wenzhu Zhang

  2. No. 1 School of Clinical Medicine, Kunming Medical University, Kunming, China

    Biqing Luan, Xingjia Lu, Zhiqiang Li, Hong Zhang, Jingxuan Wu, Qizhi Yang & Wenzhu Zhang

  3. Third Department of Breast Surgery, Third Affiliated Hospital, Kunming Medical University, Kunming, China

    Wenlin Chen

Authors
  1. Biqing Luan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fei Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xingjia Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhiqiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jingxuan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qizhi Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Liang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Wenzhu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Wenlin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BQL and FG: Conceptualization, Methodology, Software, Writing—Original draft preparation. ZQL and XJL: Revision of thesis writing, Organize data, Discuss the results. XJL, and LC: Data extraction. HZ, JXW, ZQL and QZY: Software, Validation. WLC: Writing—Reviewing and Editing. All authors did literature research. All authors contributed to the article and endorsed the submitted version.

Corresponding author

Correspondence to Wenlin Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical approval

This article does not include any studies with human participants or animals performed by any of the authors.

Informed consent

This is a systematic review and meta-analysis article that does not need informed consent or any ethical approvals in its current form.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 21 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luan, B., Ge, F., Lu, X. et al. Changes in the fecal microbiota of breast cancer patients based on 16S rRNA gene sequencing: a systematic review and meta-analysis. Clin Transl Oncol (2024). https://doi.org/10.1007/s12094-023-03373-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12094-023-03373-5

Keywords

Search

Navigation