The DOI matches its Crossref record; 53 of the 53 references it cites were found in a registry or an index.
The Microbiota of Breast Tissue and Its Association with Breast Cancer
Open accessAbstract
UNLABELLED: In the United States, 1 in 8 women will be diagnosed with breast cancer in her lifetime. Along with genetics, the environment contributes to disease development, but what these exact environmental factors are remains unknown. We have previously shown that breast tissue is not sterile but contains a diverse population of bacteria. We thus believe that the host's local microbiome could be modulating the risk of breast cancer development. Using 16S rRNA amplicon sequencing, we show that bacterial profiles differ between normal adjacent tissue from women with breast cancer and tissue from healthy controls. Women with breast cancer had higher relative abundances of Bacillus, Enterobacteriaceae and Staphylococcus Escherichia coli (a member of the Enterobacteriaceae family) and Staphylococcus epidermidis, isolated from breast cancer patients, were shown to induce DNA double-stranded breaks in HeLa cells using the histone-2AX (H2AX) phosphorylation (γ-H2AX) assay. We also found that microbial profiles are similar between normal adjacent tissue and tissue sampled directly from the tumor. This study raises important questions as to what role the breast microbiome plays in disease development or progression and how we can manipulate this for possible therapeutics or prevention. IMPORTANCE: This study shows that different bacterial profiles in breast tissue exist between healthy women and those with breast cancer. Higher relative abundances of bacteria that had the ability to cause DNA damage in vitro were detected in breast cancer patients, as was a decrease in some lactic acid bacteria, known for their beneficial health effects, including anticarcinogenic properties. This study raises important questions as to the role of the mammary microbiome in modulating the risk of breast cancer development.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“However, other studies have indeed shown cultivable bacteria in breast (127–129), lung (18), prostate (130, 131), pancreas (14, 15), and colon cancers (19, 132)”
From The microbiome and human cancer (2021) · cites this paper as [128]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887
Search and clustering orders of magnitude faster than BLAST
Edgar, R. C. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq461 · Cited by 21,098
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
Edgar, R. C. (2004) · BMC Bioinformatics · doi:10.1186/1471-2105-5-113 · Cited by 9,119
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
Lozupone, C., & Knight, R. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8228-8235.2005 · Cited by 8,227
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823
Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J., & Glöckner, F. O. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm864 · Cited by 6,682
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
Price, M. N., Dehal, P. S., & Arkin, A. P. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp077 · Cited by 5,602
Frank, D. N., St. Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., & Pace, N. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706625104 · Cited by 4,611
The Statistical Analysis of Compositional Data
Aitchison, J. (1986) · doi:10.1007/978-94-009-4109-0 · Cited by 4,383
The Statistical Analysis of Compositional Data
Piepel, G. F., & Aitchison, J. (1988) · Technometrics · doi:10.2307/1270335 · Cited by 3,451
Gut Microbiota in Human Adults with Type 2 Diabetes Differs from Non-Diabetic Adults
Larsen, N., Vogensen, F. K., van den Berg, F. W. J., Nielsen, D. S., Andreasen, A. S., Pedersen, B. K., Al-Soud, W. A., Sørensen, S. J., Hansen, L. H., & Jakobsen, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009085 · Cited by 2,952
The gut microbiota, bacterial metabolites and colorectal cancer
Louis, P., Hold, G. L., & Flint, H. J. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3344 · Cited by 2,925
DNA double-strand breaks: signaling, repair and the cancer connection
Khanna, K. K., & Jackson, S. P. (2001) · Nature Genetics · doi:10.1038/85798 · Cited by 2,455
Genomic instability — an evolving hallmark of cancer
Negrini, S., Gorgoulis, V. G., & Halazonetis, T. D. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2858 · Cited by 2,397
Intestinal inflammation targets cancer-inducing activity of the microbiota
Arthur, J. C., Perez-Chanona, E., Mühlbauer, M., Tomkovich, S., Uronis, J. M., Fan, T.-J., Campbell, B. J., Abujamel, T., Dogan, B., Rogers, A. B., et al. (2012) · Science · doi:10.1126/science.1224820 · Cited by 2,263
Disordered Microbial Communities in Asthmatic Airways
Hilty, M., Burke, C. M., Pedro, H., Cárdenas, P., Bush, A., Bossley, C. J., Davies, J. C., Ervine, A., Poulter, L. W., Pachter, L. S., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008578 · Cited by 1,874
Schwabe, R. F., & Jobin, C. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3610 · Cited by 1,689
Periodontitis: a polymicrobial disruption of host homeostasis
Darveau, R. P. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2337 · Cited by 1,688
Fernandes, A. D., Reid, J. N., Macklaim, J. M., McMurrough, T. A., Edgell, D. R., & Gloor, G. B. (2014) · Microbiome · doi:10.1186/2049-2618-2-15 · Cited by 1,329
Self-citationStructural segregation of gut microbiota between colorectal cancer patients and healthy volunteers
Wang, T., Cai, G., Qiu, Y., Fei, N., Zhang, M., Pang, X., Jia, W., Cai, S., & Zhao, L. (2012) · The ISME Journal · doi:10.1038/ismej.2011.109 · Cited by 1,287
Imai, K., Matsuyama, S., Miyaké, S., Suga, K., & Nakachi, K. (2000) · The Lancet · doi:10.1016/s0140-6736(00)03231-1 · Cited by 1,189
Escherichia coli Induces DNA Double-Strand Breaks in Eukaryotic Cells
Nougayrède, J.-P., Homburg, S., Taieb, F., Boury, M., Brzuszkiewicz, E., Gottschalk, G., Buchrieser, C., Hacker, J., Dobrindt, U., & Oswald, E. (2006) · Science · doi:10.1126/science.1127059 · Cited by 1,188
Associating microbiome composition with environmental covariates using generalized UniFrac distances
Chen, J., Bittinger, K. L., Charlson, E. S., Hoffmann, C., Lewis, J. D., Wu, G. D., Collman, R. G., Bushman, F. D., & Li, H. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts342 · Cited by 1,160
Communicable Ulcerative Colitis Induced by T-bet Deficiency in the Innate Immune System
Garrett, W. S., Lord, G. M., Punit, S., Lugo‐Villarino, G., Mazmanian, S. K., Ito, S., Glickman, J. N., & Glimcher, L. H. (2007) · Cell · doi:10.1016/j.cell.2007.08.017 · Cited by 915
Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County
Shimizu, H., Ross, R., Bernstein, L., Yatani, R., Henderson, B. E., & Mack, T. (1991) · British Journal of Cancer · doi:10.1038/bjc.1991.210 · Cited by 890
Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells
Cuevas-Ramos, G., Petit, C. R., Marcq, I., Boury, M., Oswald, E., & Nougayrède, J.-P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1001261107 · Cited by 855
Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults
Weir, T. L., Manter, D. K., Sheflin, A. M., Barnett, B. A., Heuberger, A. L., & Ryan, E. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070803 · Cited by 642
The Gut Microbiome Modulates Colon Tumorigenesis
Zackular, J. P., Baxter, N. T., Iverson, K. D., Sadler, W. D., Petrosino, J. F., Chen, G. Y., & Schloss, P. D. (2013) · mBio · doi:10.1128/mbio.00692-13 · Cited by 629
Propionate as a health-promoting microbial metabolite in the human gut
Hosseini, E., Grootaert, C., Verstraete, W., & de Wiele, T. V. (2011) · Nutrition Reviews · doi:10.1111/j.1753-4887.2011.00388.x · Cited by 586
Comparison of the microbiota of supra‐ and subgingival plaque in health and periodontitis
Ximenez‐Fyvie, L., Haffajee, A. D., & Socransky, S. S. (2000) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2000.027009648.x · Cited by 577
Microbiota of Human Breast Tissue
Urbaniak, C., Cummins, J., Brackstone, M., Macklaim, J. M., Gloor, G. B., Baban, C. K., Scott, L., O'Hanlon, D. M., Burton, J. P., Francis, K. P., et al. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.00242-14 · Cited by 552
Self-citationHigh Prevalence of Mucosa-Associated E. coli Producing Cyclomodulin and Genotoxin in Colon Cancer
Buc, E., Dubois, D., Sauvanet, P., Raisch, J., Delmas, J., Darfeuille-Michaud, A., Pezet, D., & Bonnet, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056964 · Cited by 535
Mager, D. L., Haffajee, A. D., Devlin, P. M., Norris, C., Posner, M., & Goodson, J. (2005) · Journal of Translational Medicine · doi:10.1186/1479-5876-3-27 · Cited by 516
Substantial Alterations of the Cutaneous Bacterial Biota in Psoriatic Lesions
Gao, Z., Tseng, C., Strober, B. E., Pei, Z., & Blaser, M. J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002719 · Cited by 449
Aldunate, M., Srbinovski, D., Hearps, A. C., Latham, C. F., Ramsland, P. A., Gugasyan, R., Cone, R. A., & Tachedjian, G. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00164 · Cited by 395
Repair of DNA double strand breaks by non-homologous end joining
Lees‐Miller, S. P. (2003) · Biochimie · doi:10.1016/j.biochi.2003.10.011 · Cited by 378
Toller, I. M., Neelsen, K. J., Steger, M., Hartung, M. L., Hottiger, M. O., Stucki, M., Kalali, B. N., Gerhard, M., Sartori, A. A., Lopes, M., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100959108 · Cited by 339
Local bacteria affect the efficacy of chemotherapeutic drugs
Lehouritis, P., Cummins, J., Stanton, M., Murphy, C. T., McCarthy, F. O., Reid, G., Urbaniak, C., Byrne, W. L., & Tangney, M. (2015) · Scientific Reports · doi:10.1038/srep14554 · Cited by 313
Self-citationZhao, N., Chen, J., Carroll, I. M., Ringel-Kulka, T., Epstein, M. P., Zhou, H., Zhou, J. J., Ringel, Y., Li, H., & Wu, M. C. (2015) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2015.04.003 · Cited by 306
Mira‐Pascual, L., Cabrera‐Rubio, R., Ocon, S. M., Costales, P., Parra, A., Suárez, A., Morís, F., Rodrigo, L., Mira, Á., & Collado, M. C. (2014) · Journal of Gastroenterology · doi:10.1007/s00535-014-0963-x · Cited by 269
Deep Sequencing of the Vaginal Microbiota of Women with HIV
Hummelen, R., Fernandes, A. D., Macklaim, J. M., Dickson, R. J., Changalucha, J. M., Gloor, G. B., & Reid, G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012078 · Cited by 259
Self-citationOral microbiome and oral and gastrointestinal cancer risk
Ahn, J., Chen, C. Y., & Hayes, R. B. (2012) · Cancer Causes & Control · doi:10.1007/s10552-011-9892-7 · Cited by 246
Carrega, P., Bonaccorsi, I., Carlo, E. D., Morandi, B., Paul, P., Rizzello, V., Cipollone, G., Navarra, G., Mingari, M. C., Moretta, L., et al. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1301889 · Cited by 221
Consumption of fermented milk products and breast cancer: a case-control study in The Netherlands.
Veer, P. V. ’., Dekker, J. M., Lamers, J. W. J., Kok, F. J., Schouten, E. G., Brants, H. A. M., STURMANS, F., & Hermus, R. J. J. (1989) · PubMed · Cited by 180
Wiebe, J. P., Muzia, D., Hu, J. J., Szwajcer, D., Hill, S. A., & Seachrist, J. L. (2000) · PubMed · Cited by 114
Progesterone metabolites in breast cancer
Wiebe, J. P. (2006) · Endocrine Related Cancer · doi:10.1677/erc.1.01010 · Cited by 104
Strayer, D. R., Carter, W. A., Sd, M., Pequignot, E. C., & Brodsky, I. (1984) · PubMed · Cited by 103
Impact of lactic acid bacteria on oxidative DNA damage in human derived colon cells
Koller, V. J., Marian, B., Stidl, R., Nersesyan, A. K., Winter, H., Simic, T. P., Sontag, G., & Knasmüller, S. (2007) · Food and Chemical Toxicology · doi:10.1016/j.fct.2007.09.005 · Cited by 89
de Moreno de LeBlanc, A., Matar, C., Thériault, C., & Perdigón, G. (2005) · Immunobiology · doi:10.1016/j.imbio.2005.05.024 · Cited by 85
Cancer incidence patterns among Vietnamese in the United States and Ha Noi, Vietnam
Le, G. M., Gomez, S. L., Clarke, C. A., Glaser, S. L., & West, D. W. (2002) · International Journal of Cancer · doi:10.1002/ijc.10725 · Cited by 72
Kosaka, A., Yan, H., Ohashi, S., Gotoh, Y., Sato, A., Tsutsui, H., Kaisho, T., Toda, T., & Tsuji, N. M. (2012) · International Immunopharmacology · doi:10.1016/j.intimp.2012.10.007 · Cited by 62
Shiou, S., Yu, Y., Guo, Y., He, S.-M., Mziray-Andrew, C. H., Hoenig, J. D., Sun, J., Petrof, E. O., & Claud, E. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065108 · Cited by 59
Ojanotko-Harri, A., Nikkari, T., Harrl, M., & PAUNIO, K. U. (1990) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.1990.tb00653.x · Cited by 23
Flagged first, then by citations
Cited by
Sorted by citations
The human tumor microbiome is composed of tumor type–specific intracellular bacteria
Nejman, D., Livyatan, I., Fuks, G., Gavert, N., Zwang, Y., Geller, L. T., Rotter-Maskowitz, A., Weiser, R., Mallel, G., Gigi, E., et al. (2020) · Science · doi:10.1126/science.aay9189 · Cited by 2,464
The microbiome and human cancer
Sepich-Poore, G. D., Zitvogel, L., Straussman, R., Hasty, J., Wargo, J. A., & Knight, R. (2021) · Science · doi:10.1126/science.abc4552 · Cited by 1,332
The microbiome, cancer, and cancer therapy
Helmink, B. A., Khan, M. A. W., Hermann, A., Gopalakrishnan, V., & Wargo, J. A. (2019) · Nature Medicine · doi:10.1038/s41591-019-0377-7 · Cited by 1,200
Tumor-resident intracellular microbiota promotes metastatic colonization in breast cancer
Fu, A., Yao, B., Dong, T., Chen, Y., Yao, J., Liu, Y., Li, H., Bai, H., Liu, X., Zhang, Y., et al. (2022) · Cell · doi:10.1016/j.cell.2022.02.027 · Cited by 981
Tumor biomarkers for diagnosis, prognosis and targeted therapy
Zhou, Y., Tao, L., Qiu, J., Xu, J., Yang, X., Zhang, Y., Tian, X., Guan, X., Cen, X., & Zhao, Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01823-2 · Cited by 836
Metadata
- Authors
- Urbaniak, C., Gloor, G. B., Brackstone, M., Scott, L., Tangney, M., & Reid, G.
- Affiliations
- Western University (CA)
- London Regional Cancer Program, London, Ontario, Canada
- University College Cork (IE)
- Corresponding author
- Reid, Gregor
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2016-08-15
- Volume
- 82
- Issue
- 16
- Pages
- 5039-5048
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC4968547
- OpenAlex
- W2493607481
- Cited by
- 625
- References
- 53
- Citations by year
- 2026: 51 · 2025: 102 · 2024: 75 · 2023: 82 · 2022: 68 · 2021: 88 · 2020: 63 · 2019: 41 · 2018: 29 · 2017: 19 · 2016: 5
- FWCI
- 16.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Applied and Environmental Microbiology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Arrow@dit (Dublin Institute of Technology) (submittedVersion, cc-by)
- Cork Open Research Archive (University College Cork, Ireland) (submittedVersion, cc-by)
- Scholarship@Western (Western University) (submittedVersion)
- Funders
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Keywords
- breast microbiome, breast cancer, bacterial diversity, adjacent normal tissue, tumor tissue, Bacillus, Enterobacteriaceae, Staphylococcus epidermidis, Escherichia coli, DNA double-strand breaks, H2AX phosphorylation, lactic acid bacteria, cancer risk, environmental factors
- MeSH terms
- Adult, Aged, Aged, 80 and over, Bacteria, Breast, Breast Neoplasms, Female, Humans, Middle Aged, Ontario, RNA, Ribosomal, 16S, Sequence Analysis, DNA, Young Adult, Microbiota
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review