Skip to main content

Advertisement

Springer Nature Link
Log in

Gut microbiome, body weight, and mammographic breast density in healthy postmenopausal women

  • Original Paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Purpose

We examined gut microbiome (GM) profiles in relation to mammographic breast density (BD) and body mass index (BMI) in healthy postmenopausal women.

Methods

Eligible women were postmenopausal, had a BMI ≤ 35 kg/m2, and had not recently taken oral/IV antibiotics. All women provided a fecal sample and information on breast cancer risk factors. Mammographic BD was classified with the American College of Radiology’s BI-RADS BD classification system. Bacterial DNA was isolated from fecal samples and the V1–V2 hypervariable regions of 16S rRNA were sequenced on the Illumina MiSeq platform. We examined associations of GM with indices of within-sample (alpha) diversity and the ratio of the two main phyla (Firmicutes and Bacteroidetes; F/B ratio) with BD and BMI.

Results

Among 69 women with BD data, 39 had low BD (BI-RADS I/II) and 30 had high BD (BI-RADS III/IV). BMI was inversely associated with BD (mean BMI = 23.8 and 28.0 in women with high and low BD, respectively, p = 1.07 × 10–5). Similar levels of GM diversity were found across weight groups according to Shannon (p = 0.83); Inverse Simpson (p = 0.97); and Chao1 (p = 0.31) indices. F/B ratio and microbiota diversity were suggestively greater in women with high vs. low BD (p = 0.35, 0.14, 0.15, and 0.17 for F/B ratio, Shannon, Inverse Simpson and Chao1, respectively).

Conclusion

Suggestive differences observed in women with high and low BD with respect to GM alpha diversity and prevalence of specific GM taxa need to be confirmed in larger studies.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  1. Grice EA, Segre JA (2012) The human microbiome: our second genome. Annu Rev Genomics Hum Genet 13:151–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Tilg H, Kaser A (2011) Gut microbiome, obesity, and metabolic dysfunction. J Clin Invest 121:2126–2132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kinross JM, Darzi AW, Nicholson JK (2011) Gut microbiome-host interactions in health and disease. Genome medicine 3:14

    Article  PubMed  PubMed Central  Google Scholar 

  4. Prakash S, Rodes L, Coussa-Charley M, Tomaro-Duchesneau C (2011) Gut microbiota: next frontier in understanding human health and development of biotherapeutics. Biologics 5:71–86

    PubMed  PubMed Central  Google Scholar 

  5. Sommer F, Backhed F (2013) The gut microbiota–masters of host development and physiology. Nat Rev Microbiol 11:227–238

    Article  CAS  PubMed  Google Scholar 

  6. Schwabe RF, Jobin C (2013) The microbiome and cancer. Nat Rev Cancer 13:800–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. McCormack VA, dos Santos SI (2006) Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 15:1159–1169

    Article  PubMed  Google Scholar 

  8. Jackson VP, Hendrick RE, Feig SA, Kopans DB (1993) Imaging of the radiographically dense breast. Radiology 188:297–301

    Article  CAS  PubMed  Google Scholar 

  9. Kerlikowske K, Grady D, Barclay J, Sickles EA, Ernster V (1996) Effect of age, breast density, and family history on the sensitivity of first screening mammography. JAMA 276:33–38

    Article  CAS  PubMed  Google Scholar 

  10. Kolb TM, Lichy J, Newhouse JH (2002) Comparison of the performance of screening mammography, physical examination, and breast US and evaluation of factors that influence them: an analysis of 27,825 patient evaluations. Radiology 225:165–175

    Article  PubMed  Google Scholar 

  11. Pinsky RW, Helvie MA (2010) Mammographic breast density: effect on imaging and breast cancer risk. J Natl Compr Cancer Netw 8:1157–1164

    Article  Google Scholar 

  12. Lindgren J, Dorgan J, Savage-Williams J, Coffman D, Hartman T (2013) Diet across the lifespan and the association with breast density in adulthood. Int J Breast Cancer 2013:808317

    Article  PubMed  PubMed Central  Google Scholar 

  13. Shapira I, Sultan K, Lee A, Taioli E (2013) Evolving concepts: how diet and the intestinal microbiome act as modulators of breast malignancy. ISRN Oncol 2013:693920

    PubMed  PubMed Central  Google Scholar 

  14. Chang S-C, Ziegler RG, Dunn B et al (2006) Association of energy intake and energy balance with postmenopausal breast cancer in the prostate, lung, colorectal, and ovarian cancer screening trial. Cancer Epidemiol Biomarkers Prev 15:334–341

    Article  PubMed  Google Scholar 

  15. Ferrari P, Rinaldi S, Jenab M et al (2013) Dietary fiber intake and risk of hormonal receptor-defined breast cancer in the European Prospective Investigation into Cancer and Nutrition study. Am J Clin Nutr 97:344–353

    Article  CAS  PubMed  Google Scholar 

  16. Kushi LH, Sellers TA, Potter JD et al (1992) Dietary fat and postmenopausal breast cancer. J Natl Cancer Inst 84:1092–1099

    Article  CAS  PubMed  Google Scholar 

  17. Thomson CA (2012) Diet and breast cancer: understanding risks and benefits. Nutr Clin Pract 27:636–650

    Article  PubMed  Google Scholar 

  18. Zaineddin AK, Buck K, Vrieling A et al (2012) The association between dietary lignans, phytoestrogen-rich foods, and fiber intake and postmenopausal breast cancer risk: a German case-control study. Nutr Cancer 64:652–665

    Article  CAS  PubMed  Google Scholar 

  19. Zhang CX, Ho SC, Cheng SZ, Chen YM, Fu JH, Lin FY (2011) Effect of dietary fiber intake on breast cancer risk according to estrogen and progesterone receptor status. Eur J Clin Nutr 65:929–936

    Article  PubMed  Google Scholar 

  20. Ericson U, Borgquist S, Ivarsson MIL et al (2010) Plasma folate concentrations are positively associated with risk of estrogen receptor β negative breast cancer in a Swedish nested case control study. J Nutr 140:1661–1668

    Article  CAS  PubMed  Google Scholar 

  21. Fung TT, Hu FB, McCullough ML, Newby PK, Willett WC, Holmes MD (2006) Diet quality is associated with the risk of estrogen receptor-negative breast cancer in postmenopausal women. J Nutr 136:466–472

    Article  CAS  PubMed  Google Scholar 

  22. Larsson SC, Giovannucci E, Wolk A (2007) Folate and risk of breast cancer: a meta-analysis. J Natl Cancer Inst 99:64–76

    Article  CAS  PubMed  Google Scholar 

  23. Park Y, Brinton LA, Subar AF, Hollenbeck A, Schatzkin A (2009) Dietary fiber intake and risk of breast cancer in postmenopausal women: the National Institutes of Health-AARP Diet and Health Study. Am J Clin Nutr 90:664–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mishra G, dos Santos SI, McNaughton S, Stephen A, Kuh D (2011) Energy intake and dietary patterns in childhood and throughout adulthood and mammographic density: results from a British prospective cohort. Cancer Causes Control 22:227–235

    Article  PubMed  Google Scholar 

  25. Vachon CM, Kushi LH, Cerhan JR, Kuni CC, Sellers TA (2000) Association of diet and mammographic breast density in the Minnesota breast cancer family cohort. Cancer Epidemiol Biomarkers Prev 9:151–160

    CAS  PubMed  Google Scholar 

  26. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA et al (2009) High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137:1716–24.e2

    Article  CAS  PubMed  Google Scholar 

  27. Muegge BD, Kuczynski J, Knights D et al (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1:6ra14

    Article  PubMed  PubMed Central  Google Scholar 

  29. Ahn J, Sinha R, Pei Z et al (2013) Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst 105:1907–1911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Soguel L, Durocher F, Tchernof A, Diorio C (2017) Adiposity, breast density, and breast cancer risk: epidemiological and biological considerations. Eur J Cancer Prev 26:511–520

    Article  PubMed  PubMed Central  Google Scholar 

  31. Jones GS, Spencer Feigelson H, Falk RT et al (2019) Mammographic breast density and its association with urinary estrogens and the fecal microbiota in postmenopausal women. PLoS ONE 14:e0216114

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rowe RW, Tomoda M, Strebel FR, Jenkins GN, Stephens LC, Bull JM (2004) The natural progression of microvasculature in primary tumor and lymph node metastases in a breast carcinoma model: relationship between microvessel density, vascular endothelial growth factor expression, and metastatic invasion. Cancer Biol Ther 3:408–414

    Article  CAS  PubMed  Google Scholar 

  33. Brenner PF, Goebelsmann U, Stanczyk FZ, Mishell DR Jr (1980) Serum levels of ethinylestradiol following its ingestion alone or in oral contraceptive formulations. Contraception 22:85–95

    Article  CAS  PubMed  Google Scholar 

  34. Razzaghi H, Troester MA, Gierach GL, Olshan AF, Yankaskas BC, Millikan RC (2012) Mammographic density and breast cancer risk in White and African American Women. Breast Cancer Res Treat 135:571–580

    Article  PubMed  PubMed Central  Google Scholar 

  35. Kerlikowske K, Zhu W, Tosteson AN et al (2015) Identifying women with dense breasts at high risk for interval cancer: a cohort study. Ann Intern Med 162:673–681

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kerlikowske K, Ma L, Scott CG et al (2017) Combining quantitative and qualitative breast density measures to assess breast cancer risk. Breast Cancer Res 19:97

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ziv E, Shepherd J, Kerlikowske K, Smith-Bindman R (2003) Mammographic breast density and family history of breast cancer. J Natl Cancer Inst 95:556–558

    Article  PubMed  Google Scholar 

  38. Ziv E, Tice J, Smith-Bindman R, Shepherd J, Cummings S, Kerlikowske K (2004) Mammographic density and estrogen receptor status of breast cancer. Cancer Epidemiol Biomarkers Prev 13:2090–2095

    Article  CAS  PubMed  Google Scholar 

  39. White AJ, Weinberg CR, O’Meara ES, Sandler DP, Sprague BL (2019) Airborne metals and polycyclic aromatic hydrocarbons in relation to mammographic breast density. Breast Cancer Res 21:24

    Article  PubMed  PubMed Central  Google Scholar 

  40. Rutter CM, Mandelson MT, Laya MB, Taplin S (2001) Changes in breast density associated with initiation, discontinuation, and continuing use of hormone replacement therapy. JAMA 285:171–176

    Article  CAS  PubMed  Google Scholar 

  41. Aiello EJ, Buist DSM, White E, Porter PL (2005) Association between mammographic breast density and breast cancer tumor characteristics. Cancer Epidemiol Biomarkers Prev 14:662–668

    Article  PubMed  Google Scholar 

  42. Harvey JA, Bovbjerg VE, Smolkin ME, Williams MB, Petroni GR (2005) Evaluating hormone therapy-associated increases in breast density: comparison between reported and simultaneous assignment of BI-RADS categories, visual assessment, and quantitative analysis1. Acad Radiol 12:853–862

    Article  PubMed  Google Scholar 

  43. van der Waal D, den Heeten GJ, Pijnappel RM et al (2015) Comparing visually assessed BI-RADS breast density and automated volumetric breast density software: a cross-sectional study in a breast cancer screening setting. PLoS ONE 10:e0136667

    Article  PubMed  PubMed Central  Google Scholar 

  44. Spayne MC, Gard CC, Skelly J, Miglioretti DL, Vacek PM, Geller BM (2012) Reproducibility of BI-RADS breast density measures among community radiologists: a prospective cohort study. Breast J 18:326–333

    Article  PubMed  PubMed Central  Google Scholar 

  45. Ciatto S, Houssami N, Apruzzese A et al (2005) Categorizing breast mammographic density: intra- and inter-observer reproducibility of BI-RADS density categories. Breast 14:269–275

    Article  CAS  PubMed  Google Scholar 

  46. Kerlikowske K, Grady D, Barclay J et al (1998) Variability and accuracy in mammographic interpretation using the American College of Radiology Breast Imaging Reporting and Data System. J Natl Cancer Inst 90:1801–1809

    Article  CAS  PubMed  Google Scholar 

  47. Gweon HM, Youk JH, Kim J-A, Son EJ (2013) Radiologist assessment of breast density by BI-RADS categories versus fully automated volumetric assessment. Am J Roentgenol 201:692–697

    Article  Google Scholar 

  48. Winkel RR, von Euler-Chelpin M, Nielsen M et al (2015) Inter-observer agreement according to three methods of evaluating mammographic density and parenchymal pattern in a case control study: impact on relative risk of breast cancer. BMC Cancer 15:274

    Article  PubMed  PubMed Central  Google Scholar 

  49. Jamal N, Ng KH, Looi LM et al (2006) Quantitative assessment of breast density from digitized mammograms into Tabar’s patterns. Phys Med Biol 51:5843–5857

    Article  CAS  PubMed  Google Scholar 

  50. Jeffreys M, Warren R, Smith GD, Gunnell D (2003) Breast density: agreement of measures from film and digital image. Br J Radiol 76:561–563

    Article  CAS  PubMed  Google Scholar 

  51. Prevrhal S, Shepherd JA, Smith-Bindman R, Cummings SR, Kerlikowske K (2002) Accuracy of mammographic breast density analysis: results of formal operator training. Cancer Epidemiol Biomarkers Prev 11:1389–1393

    PubMed  Google Scholar 

  52. Youk JH, Kim SJ, Son EJ, Gweon HM, Kim J-A (2017) Comparison of visual assessment of breast density in BI-RADS 4th and 5th editions with automated volumetric measurement. Am J Roentgenol 209:703–708

    Article  Google Scholar 

  53. Kerlikowske K, Scott CG, Mahmoudzadeh AP et al (2018) Automated and clinical breast imaging reporting and data system density measures predict risk for screen-detected and interval cancers: a case-control study. Ann Intern Med 168:757–765

    Article  PubMed  PubMed Central  Google Scholar 

  54. Klann E, Williamson JM, Tagliamonte MS et al (2020) Microbiota composition in bilateral healthy breast tissue and breast tumors. Cancer Causes Control 31:1027–1038

    Article  PubMed  Google Scholar 

  55. Miller DN, Bryant JE, Madsen EL, Ghiorse WC (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65:4715–4724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zoetendal EG, Akkermans AD, De Vos WM (1998) Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 64:3854–3859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:235–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sun Y, Cai Y, Huse SM et al (2012) A large-scale benchmark study of existing algorithms for taxonomy-independent microbial community analysis. Brief Bioinform 13:107–121

    Article  PubMed  Google Scholar 

  59. Sun Y, Cai Y, Mai V et al (2010) Advanced computational algorithms for microbial community analysis using massive 16S rRNA sequence data. Nucleic Acids Res 38:e205

    Article  PubMed  PubMed Central  Google Scholar 

  60. Cai Y, Sun Y (2011) ESPRIT-Tree: hierarchical clustering analysis of millions of 16S rRNA pyrosequences in quasilinear computational time. Nucleic Acids Res 39:e95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Pylro VS, Roesch LF, Ortega JM et al (2014) Brazilian Microbiome Project: revealing the unexplored microbial diversity–challenges and prospects. Microb Ecol 67:237–241

    Article  PubMed  Google Scholar 

  63. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Willett W, Stampfer MJ, Bain C et al (1983) Cigarette smoking, relative weight, and menopause. Am J Epidemiol 117:651–658

    Article  CAS  PubMed  Google Scholar 

  65. Stampfer MJ, Willett WC, Colditz GA, Rosner B, Speizer FE, Hennekens CH (1985) A prospective study of postmenopausal estrogen therapy and coronary heart disease. N Engl J Med 313:1044–1049

    Article  CAS  PubMed  Google Scholar 

  66. Kim BR, Shin J, Guevarra R et al (2017) Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol 27:2089–2093

    Article  PubMed  Google Scholar 

  67. Reese AT, Dunn RR (2018) Drivers of microbiome biodiversity: a review of general rules, feces, and ignorance. MBio 9:e01294–e01318

    Article  PubMed  PubMed Central  Google Scholar 

  68. Kerlikowske K, Cook AJ, Buist DS et al (2010) Breast cancer risk by breast density, menopause, and postmenopausal hormone therapy use. J Clin Oncol 28:3830–3837

    Article  PubMed  PubMed Central  Google Scholar 

  69. Vacek PM, Geller BM (2004) A prospective study of breast cancer risk using routine mammographic breast density measurements. Cancer Epidemiol Biomarkers Prev 13:715–722

    Article  PubMed  Google Scholar 

  70. Kerlikowske K, Ichikawa L, Miglioretti DL et al (2007) Longitudinal measurement of clinical mammographic breast density to improve estimation of breast cancer risk. J Natl Cancer Inst 99:386–395

    Article  PubMed  Google Scholar 

  71. Gierach GL, Ichikawa L, Kerlikowske K et al (2012) Relationship between mammographic density and breast cancer death in the breast cancer surveillance consortium. JNCI J Natl Cancer Inst 104:1218–1227

    Article  PubMed  Google Scholar 

  72. Sprague BL, Gangnon RE, Burt V et al (2014) Prevalence of mammographically dense breasts in the United States. J Natl Cancer Inst 106:dju255

    Article  PubMed  PubMed Central  Google Scholar 

  73. Lowry SJ, Sprague BL, Aiello Bowles EJ et al (2012) Mammographic breast density and serum phytoestrogen levels. Nutr Cancer 64:783–789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Sprague BL, Trentham-Dietz A, Hedman CJ et al (2013) Circulating serum xenoestrogens and mammographic breast density. Breast Cancer Res 15:R45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Belkaid Y, Hand TW (2014) Role of the microbiota in immunity and inflammation. Cell 157:121–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Scher JU, Littman DR, Abramson SB (2016) Microbiome in Inflammatory Arthritis and Human Rheumatic Diseases. Arthritis Rheumatol 68:35–45

    Article  PubMed  PubMed Central  Google Scholar 

  77. Kamada N, Seo SU, Chen GY, Nunez G (2013) Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 13:321–335

    Article  CAS  PubMed  Google Scholar 

  78. Cenit MC, Matzaraki V, Tigchelaar EF, Zhernakova A (2014) Rapidly expanding knowledge on the role of the gut microbiome in health and disease. Biochem Biophys Acta 1842:1981–1992

    CAS  PubMed  Google Scholar 

  79. Terry MB, Buist DS, Trentham-Dietz A, James-Todd TM, Liao Y (2008) Nonsteroidal anti-inflammatory drugs and change in mammographic density: a cohort study using pharmacy records on over 29,000 postmenopausal women. Cancer Epidemiol Biomarkers Prev 17:1088–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Maskarinec G, Urano Y, Gill J, Kolonel LN (2008) Nonsteroidal anti-inflammatory drugs (NSAIDs) and mammographic density. Breast Cancer Res Treat 112:133–139

    Article  CAS  PubMed  Google Scholar 

  81. Reeves KW, Weissfeld JL, Modugno F, Diergaarde B (2011) Circulating levels of inflammatory markers and mammographic density among postmenopausal women. Breast Cancer Res Treat 127:555–563

    Article  CAS  PubMed  Google Scholar 

  82. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031

    Article  PubMed  Google Scholar 

  83. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3:213–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Turnbaugh PJ, Hamady M, Yatsunenko T et al (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484

    Article  CAS  PubMed  Google Scholar 

  85. Flores R, Shi J, Gail MH, Gajer P, Ravel J, Goedert JJ (2012) Assessment of the human faecal microbiota: II. Reproducibility and associations of 16S rRNA pyrosequences. Eur J Clin Invest 42:855–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Keum N, Greenwood DC, Lee DH et al (2015) Adult weight gain and adiposity-related cancers: a dose-response meta-analysis of prospective observational studies. J Natl Cancer Inst 107:djv088

    Article  PubMed  Google Scholar 

  87. Cani PD (2013) Gut microbiota and obesity: lessons from the microbiome. Brief Funct Genomics 12:381–387

    Article  CAS  PubMed  Google Scholar 

  88. Dugas LR, Fuller M, Gilbert J, Layden BT (2016) The obese gut microbiome across the epidemiologic transition. Emerg Themes Epidemiol 13:2

    Article  PubMed  PubMed Central  Google Scholar 

  89. Hankinson SE, Willett WC, Manson JE et al (1995) Alcohol, height, and adiposity in relation to estrogen and prolactin levels in postmenopausal women. J Natl Cancer Inst 87:1297–1302

    Article  CAS  PubMed  Google Scholar 

  90. Dorgan JF, Baer DJ, Albert PS et al (2001) Serum hormones and the alcohol-breast cancer association in postmenopausal women. J Natl Cancer Inst 93:710–715

    Article  CAS  PubMed  Google Scholar 

  91. Sorensen HT, Skriver MV, Friis S, McLaughlin JK, Blot WJ, Baron JA (2005) Use of antibiotics and risk of breast cancer: a population-based case-control study. Br J Cancer 92:594–596

    Article  CAS  PubMed  Google Scholar 

  92. Garcia Rodriguez LA, Gonzalez-Perez A (2005) Use of antibiotics and risk of breast cancer. Am J Epidemiol 161:616–619

    Article  CAS  PubMed  Google Scholar 

  93. Castaner O, Goday A, Park YM et al (2018) The gut microbiome profile in obesity: a systematic review. Int J Endocrinol 2018:4095789

    PubMed  PubMed Central  Google Scholar 

  94. Tseng CH, Wu CY (2019) The gut microbiome in obesity. J Formosan Med Assoc 118(Suppl 1):S3–S9

    Article  PubMed  Google Scholar 

  95. Maruvada P, Leone V, Kaplan LM, Chang EB (2017) The human microbiome and obesity: moving beyond associations. Cell Host Microbe 22:589–599

    Article  CAS  PubMed  Google Scholar 

  96. Thaiss CA (2018) Microbiome dynamics in obesity. Science 362:903–904

    Article  CAS  PubMed  Google Scholar 

  97. Schieber AM, Lee YM, Chang MW et al (2015) Disease tolerance mediated by microbiome E. coli involves inflammasome and IGF-1 signaling. Science 350:558–563

    Article  CAS  PubMed  Google Scholar 

  98. Rice MS, Tamimi RM, Connolly JL et al (2012) Insulin-like growth factor-1, insulin-like growth factor binding protein-3 and lobule type in the Nurses’ Health Study II. Breast Cancer Res 14:R44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Christopoulos PF, Msaouel P, Koutsilieris M (2015) The role of the insulin-like growth factor-1 system in breast cancer. Mol Cancer 14:43

    Article  PubMed  PubMed Central  Google Scholar 

  100. Rinaldi S, Peeters PH, Berrino F et al (2006) IGF-I, IGFBP-3 and breast cancer risk in women: The European Prospective Investigation into Cancer and Nutrition (EPIC). Endocr Relat Cancer 13:593–605

    Article  CAS  PubMed  Google Scholar 

  101. Endogenous H, Breast Cancer Collaborative G, Key TJ, Appleby PN, Reeves GK, Roddam AW (2010) Insulin-like growth factor 1 (IGF1), IGF binding protein 3 (IGFBP3), and breast cancer risk: pooled individual data analysis of 17 prospective studies. Lancet Oncol 11:530–542

    Article  Google Scholar 

  102. Lagiou P, Samoli E, Lagiou A et al (2013) A comparison of hormonal profiles between breast cancer and benign breast disease: a case-control study. Ann Oncol 24:2527–2533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Su X, Colditz GA, Willett WC et al (2010) Genetic variation and circulating levels of IGF-I and IGFBP-3 in relation to risk of proliferative benign breast disease. Int J Cancer 126:180–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Rinninella E, Raoul P, Cintoni M et al (2019) What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms 7:14

    Article  CAS  PubMed Central  Google Scholar 

  105. Riva A, Borgo F, Lassandro C et al (2017) Pediatric obesity is associated with an altered gut microbiota and discordant shifts in Firmicutes populations. Environ Microbiol 19:95–105

    Article  CAS  PubMed  Google Scholar 

  106. Chambers ES, Preston T, Frost G, Morrison DJ (2018) Role of gut microbiota-generated short-chain fatty acids in metabolic and cardiovascular health. Curr Nutr Rep 7:198–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Xiao L, Sonne SB, Feng Q et al (2017) High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice. Microbiome 5:43

    Article  PubMed  PubMed Central  Google Scholar 

  108. Vital M, Karch A, Pieper DH (2017) Colonic butyrate-producing communities in humans: an overview using omics data. mSystems 2:e00130-e1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Poeker SA, Geirnaert A, Berchtold L et al (2018) Understanding the prebiotic potential of different dietary fibers using an in vitro continuous adult fermentation model (PolyFermS). Sci Rep 8:4318

    Article  PubMed  PubMed Central  Google Scholar 

  110. Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L (2016) Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 7:979

    Article  PubMed  PubMed Central  Google Scholar 

  111. Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A (2011) Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol 17:1519–1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Ghosh K, Brandt KR, Sellers TA et al (2008) Association of mammographic density with the pathology of subsequent breast cancer among postmenopausal women. Cancer Epidemiol Biomarkers Prev 17:872–879

    Article  PubMed  PubMed Central  Google Scholar 

  113. Clavel T, Lepage P, Charrier C (2014) The family Coriobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: actinobacteria. Springer, Berlin, pp 201–238

    Google Scholar 

  114. Waters JL, Ley RE (2019) The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biol 17:83

    Article  PubMed  PubMed Central  Google Scholar 

  115. Krishnan K, Baglietto L, Stone J et al (2017) Longitudinal study of mammographic density measures that predict breast cancer risk. Cancer Epidemiol Biomarkers Prev 26:651–660

    Article  PubMed  PubMed Central  Google Scholar 

  116. Brandt KR, Scott CG, Miglioretti DL et al (2019) Automated volumetric breast density measures: differential change between breasts in women with and without breast cancer. Breast Cancer Res 21:118

    Article  PubMed  PubMed Central  Google Scholar 

  117. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB (2009) Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 77:2367–2375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Caporaso JG, Lauber CL, Costello EK et al (2011) Moving pictures of the human microbiome. Genome Biol 12:R50

    Article  PubMed  PubMed Central  Google Scholar 

  119. Human Microbiome Project C (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214

    Article  Google Scholar 

  120. Faith JJ, Guruge JL, Charbonneau M et al (2013) The long-term stability of the human gut microbiota. Science 341:1237439

    Article  PubMed  PubMed Central  Google Scholar 

  121. Franzosa EA, Morgan XC, Segata N et al (2014) Relating the metatranscriptome and metagenome of the human gut. Proc Natl Acad Sci USA 111:E2329–E2338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Kerlikowske K, Vachon CM (2016) Breast density: more than meets the eye. J Natl Cancer Inst 108:djw128

    Article  PubMed  Google Scholar 

  123. Yoong SL, Carey ML, D’Este C, Sanson-Fisher RW (2013) Agreement between self-reported and measured weight and height collected in general practice patients: a prospective study. BMC Med Res Methodol 13:38

    Article  PubMed  PubMed Central  Google Scholar 

  124. Dahl AK, Hassing LB, Fransson EI, Pedersen NL (2010) Agreement between self-reported and measured height, weight and body mass index in old age: a longitudinal study with 20 years of follow-up. Age Ageing 39:445–451

    Article  PubMed  PubMed Central  Google Scholar 

  125. Lin CJ, DeRoo LA, Jacobs SR, Sandler DP (2012) Accuracy and reliability of self-reported weight and height in the Sister Study. Public Health Nutr 15:989–999

    Article  PubMed  Google Scholar 

  126. Spencer E, Appleby P, Davey G, Key T (2002) Validity of self-reported height and weight in 4808 EPIC-Oxford participants. Public Health Nutr 5:561–565

    Article  PubMed  Google Scholar 

  127. Hodge JM, Shah R, McCullough ML, Gapstur SM, Patel AV (2020) Validation of self-reported height and weight in a large, nationwide cohort of U.S. adults. PLoS ONE 15:e0231229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Florida Academic Cancer Center Alliance and UF Health Cancer Center Bridge Funding. We would like to thank participants of this study for providing the data and samples.

Author information

Authors and Affiliations

  1. Department of Epidemiology, College of Public Health and Health Professions and College of Medicine, University of Florida, Gainesville, FL, USA

    Lusine Yaghjyan, Volker Mai & Shannan N. Rich

  2. Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA

    Volker Mai, Maria Ukhanova & Maximiliano Tagliamonte

  3. H. Lee Moffitt Cancer Center, Tampa, FL, USA

    Xuefeng Wang, Yessica C. Martinez & Kathleen M. Egan

  4. Moffitt Cancer Center and Research Institute, 12902 USF Magnolia Drive, Tampa, FL, 33612, USA

    Kathleen M. Egan

Authors
  1. Lusine Yaghjyan
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Volker Mai
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Xuefeng Wang
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Maria Ukhanova
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Maximiliano Tagliamonte
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Yessica C. Martinez
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Shannan N. Rich
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Kathleen M. Egan
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Kathleen M. Egan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This study was approved by the Moffitt Cancer Center and UF Institutional Review Boards (UF: IRB 201500572 and IRB 201600709; Moffitt Cancer Center SRC 18419). The study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments.

Informed consent

All participants provided written informed consent.

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 181 KB)

Supplementary file2 (DOCX 601 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yaghjyan, L., Mai, V., Wang, X. et al. Gut microbiome, body weight, and mammographic breast density in healthy postmenopausal women. Cancer Causes Control 32, 681–692 (2021). https://doi.org/10.1007/s10552-021-01420-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-021-01420-6

Keywords