Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Communication
  • Published:

Consumption of Lactobacillus acidophilus and Bifidobacterium longum do not alter urinary equol excretion and plasma reproductive hormones in premenopausal women

European Journal of Clinical Nutrition volume 58, pages 1635–1642 (2004)Cite this article

Abstract

Objective: To confirm the results of an earlier study showing premenopausal equol excretors to have hormone profiles associated with reduced breast cancer risk, and to investigate whether equol excretion status and plasma hormone concentrations can be influenced by consumption of probiotics.

Design: A randomized, single-blinded, placebo-controlled, parallel-arm trial.

Subjects: In all, 34 of the initially enrolled 37 subjects completed all requirements.

Intervention: All subjects were followed for two full menstrual cycles and the first seven days of a third cycle. During menstrual cycle 1, plasma concentrations of estradiol (E2), estrone (E1), estrone-sulfate (E1-S), testosterone (T), androstenedione (A), dehydroepiandrosterone-sulfate (DHEA-S), and sex-hormone-binding globulin (SHBG) were measured on cycle day 2, 3, or 4, and urinary equol measured on day 7 after a 4-day soy challenge. Subjects then received either probiotic capsules (containing Lactobacillus acidophilus and Bifidobacterium longum) or placebo capsules through day 7 of menstrual cycle 3, at which time both the plasma hormone concentrations and the post-soy challenge urinary equol measurements were repeated.

Results: During menstrual cycle 1, equol excretors and non-excretors were not significantly different with respect to subject characteristics, diet, or hormone concentrations. Significant inverse correlations were found between E2 and body mass index (BMI) (P=0.02), SHBG and BMI (P=0.01), DHEA-S and dietary fiber (P=0.04), and A and protein:carbohydrate ratio (P=0.02). Probiotic consumption failed to significantly alter equol excretor status or hormone concentrations during menstrual cycle 3, although there were trends towards decreased concentrations of T (P=0.14) and SHBG (P=0.10) in the probiotic group.

Conclusions: We were unable to verify a previously reported finding of premenopausal equol excretors having plasma hormone concentrations different from those of nonexcretors. Furthermore, a 2-month intervention with probiotic capsules did not significantly alter equol excretion or plasma hormone concentrations.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  • Adlercreutz H, Hamalainen E, Gorbach SL, Goldin BR, Woods MN & Dwyer JT (1989): Diet and plasma androgens in postmenopausal vegetarian and omnivorous women and postmenopausal women with breast cancer. Am. J. Clin. Nutr. 49, 433–442.

    Article  CAS  Google Scholar 

  • Adlercreutz H, Honjo H, Higashi A, Fotsis T, Hamalainen E, Hasegawa T & Okada H (1991): Urinary excretion of lignans and isoflavonoid phytoestrogens in Japanese men and women consuming a traditional Japanese diet. Am. J. Clin. Nutr. 54, 1093–1100.

    Article  CAS  Google Scholar 

  • Anderson KE, Rosner W, Khan MS, New MI, Pang SY, Wissel PS & Kappas A (1987): Diet–hormone interactions: protein/carbohydrate ratio alters reciprocally the plasma levels of testosterone and cortisol and their respective binding globulins in man. Life Sci. 40, 1761–1768.

    Article  CAS  Google Scholar 

  • Benno Y & Mitsuoka T (1992): Impact of Bifidobacterium longum on human fecal microflora. Microbiol. Immunol. 36, 683–694.

    Article  CAS  Google Scholar 

  • Bezkorovainy A (2001): Probiotics: determinants of survival and growth in the gut. Am. J. Clin. Nutr. 73, 399S–405S.

    Article  CAS  Google Scholar 

  • Bhathena SJ, Berlin E, Judd J, Nair PP, Kennedy BW, Jones J, Smith PM, Jones Y, Taylor PR & Campbell WS (1989): Hormones regulating lipid and carbohydrate metabolism in premenopausal women: modulation by dietary lipids. Am. J. Clin. Nutr. 49, 752–757.

    Article  CAS  Google Scholar 

  • Block G, Hartmann AM, Dresser CM, Carroll MD, Gannon J & Gardner L (1986): A data-based approach to diet questionnaire design and testing. Am. J. Epidemiol 124, 453–469.

    Article  CAS  Google Scholar 

  • Brouwers E, L'Homme R, Al-Maharik N, Lapcik O, Hampl R, Wahala K, Mikola H & Adlercreutz H (2003): Time-resolved fluoroimmunoassay for equol in plasma and urine. J. Steroid Biochem. Mol. Biol. 84, 577–588.

    Article  CAS  Google Scholar 

  • Cassidy A, Bingham S & Setchell KD (1994): Biological effects of a diet of soy protein rich in isoflavones on the menstrual cycle of premenopausal women. Am. J. Clin. Nutr. 60, 333–340.

    Article  CAS  Google Scholar 

  • Dai Q, Franke AA, Jin F, Shu XO, Hebert JR, Custer LJ, Cheng J, Gao YT & Zheng W (2002): Urinary excretion of phytoestrogens and risk of breast cancer among Chinese women in Shanghai. Cancer Epidemiol. Biomarkers Prev. 11, 815–821.

    CAS  PubMed  Google Scholar 

  • Dorgan JF, Reichman ME, Judd JT, Brown C, Longcope C, Schatzkin A, Forman M, Campbell WS, Franz C, Kahle L & Taylor PR (1996): Relation of energy, fat, and fiber intakes to plasma concentrations of estrogens and androgens in premenopausal women. Am. J. Clin. Nutr. 64, 25–31.

    Article  CAS  Google Scholar 

  • Duncan AM, Merz-Demlow BE, Xu X, Phipps WR & Kurzer MS (2000): Premenopausal equol excretors show plasma hormone profiles associated with lowered risk of breast cancer. Cancer Epidemiol. Biomarkers Prev. 9, 581–586.

    CAS  PubMed  Google Scholar 

  • Franks S, Kiddy DS, Hamilton-Fairley D, Bush A, Sharp PS & Reed MJ (1991): The role of nutrition and insulin in the regulation of sex hormone binding globulin. J. Steroid Biochem. Mol. Biol. 39, 835–838.

    Article  CAS  Google Scholar 

  • Gibson GR & Roberfroid MB (1995): Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125, 1401–1412.

    Article  CAS  Google Scholar 

  • Goldin BR & Gorbach SL (1984): The effect of milk and lactobacillus feeding on human intestinal bacterial enzyme activity. Am. J. Clin. Nutr. 39, 756–761.

    Article  CAS  Google Scholar 

  • Goldin BR & Gorbach SL (1994): Hormone studies and the diet and breast cancer connection. Adv. Exp. Med. Biol. 364, 35–46.

    Article  CAS  Google Scholar 

  • Grenman S, Ronnemaa T, Irjala K, Kaihola HL & Gronroos M (1986): Sex steroid, gonadotropin, cortisol, and prolactin levels in healthy, massively obese women: correlation with abdominal fat cell size and effect of weight reduction. J. Clin. Endocrinol. Metab. 63, 1257–1261.

    Article  CAS  Google Scholar 

  • Hämäläinen EK, Adlercreutz H, Puska P & Pietinen P (1983): Decrease of serum total and free testosterone during a low-fat high-fibre diet. J. Steroid Biochem. 18, 369–370.

    Article  Google Scholar 

  • Hawksworth G, Drasar BS & Hill MJ (1971): Intestinal bacteria and the hydrolysis of glycosidic bonds. J. Med. Microbiol. 4, 451–459.

    Article  CAS  Google Scholar 

  • Hutchins AM, Slavin JL & Lampe JW (1995): Urinary isoflavonoid phytoestrogen and lignan excretion after consumption of fermented and unfermented soy products. J. Am. Diet. Assoc. 95, 545–551.

    Article  CAS  Google Scholar 

  • Ingram D, Sanders K, Kolybaba M & Lopez D (1997): Case–control study of phyto-oestrogens and breast cancer. Lancet 350, 990–994.

    Article  CAS  Google Scholar 

  • Kelly GE, Joannou GE, Reeder AY, Nelson C & Waring MA (1995): The variable metabolic response to dietary isoflavones in humans. Proc. Soc. Exp. Biol. Med. 208, 40–43.

    Article  CAS  Google Scholar 

  • Key TJ, Allen NE, Verkasalo PK & Banks E (2001): Energy balance and cancer: the role of sex hormones. Proc. Nutr. Soc. 60, 81–89.

    Article  CAS  Google Scholar 

  • Kirschner MA, Samojlik E & Silber D (1983): A comparison of androgen production and clearance in hirsute and obese women. J. Steroid Biochem. 19, 607–614.

    Article  CAS  Google Scholar 

  • Lampe JW, Gustafson DR, Hutchins AM, Martini MC, Li S, Wahala K, Grandits GA, Potter JD & Slavin JL (1999): Urinary isoflavonoid and lignan excretion on a Western diet: relation to soy, vegetable, and fruit intake. Cancer Epidemiol. Biomarkers Prev. 8, 699–707.

    CAS  PubMed  Google Scholar 

  • Lampe JW, Karr SC, Hutchins AM & Slavin JL (1998): Urinary equol excretion with a soy challenge: influence of habitual diet. Proc. Soc. Exp. Biol. Med. 217, 335–339.

    Article  CAS  Google Scholar 

  • Lampe JW, Skor HE, Li S, Wahala K, Howald WN & Chen C (2001): Wheat bran and soy protein feeding do not alter urinary excretion of the isoflavan equol in premenopausal women. J. Nutr. 131, 740–744.

    Article  CAS  Google Scholar 

  • Lee HP, Gourley L, Duffy SW, Esteve J, Lee J & Day NE (1991): Dietary effects on breast-cancer risk in Singapore. Lancet 337, 1197–1200.

    Article  CAS  Google Scholar 

  • Lu LJ, Lin SN, Grady JJ, Nagamani M & Anderson KE (1996): Altered kinetics and extent of urinary daidzein and genistein excretion in women during chronic soya exposure. Nutr. Cancer 26, 289–302.

    Article  CAS  Google Scholar 

  • Marteau P, Pochart P, Flourie B, Pellier P, Santos L, Desjeux JF & Rambaud JC (1990): Effect of chronic ingestion of a fermented dairy product containing Lactobacillus acidophilus and Bifidobacterium bifidum on metabolic activities of the colonic flora in humans. Am. J. Clin. Nutr. 52, 685–688.

    Article  CAS  Google Scholar 

  • Maskarinec G, Williams AE, Inouye JS, Stanczyk FZ & Franke AA (2002): A randomized isoflavone intervention among premenopausal women. Cancer Epidemiol. Biomarkers Prev. 11, 195–201.

    CAS  PubMed  Google Scholar 

  • Morton MS, Arisaka O, Miyake N, Morgan LD & Evans BA (2002): Phytoestrogen concentrations in serum from Japanese men and women over forty years of age. J. Nutr. 132, 3168–3171.

    Article  CAS  Google Scholar 

  • Plymate SR, Matej LA, Jones RE & Friedl KE (1988): Inhibition of sex hormone-binding globulin production in the human hepatoma (Hep G2) cell line by insulin and prolactin. J. Clin. Endocrinol. Metab. 67, 460–464.

    Article  CAS  Google Scholar 

  • Rao AV (1995): Effect of dietary fiber on intestinal microflora and health. In Dietary Fiber in Health & Disease eds D Kritchevsky and C Bonfield, pp 257–266. St. Paul: Eagan Press.

    Google Scholar 

  • Richelle M, Merten-Pridmore S, Bodenstab S, Enslen M & Offord EA (2002): Hydrolysis of isoflavone glycosides to aglycones by beta-glycosidase does not alter plasma and urine isoflavone pharmokinetics in postmenopausal women. J. Nutr. 132, 2487–2592.

    Google Scholar 

  • Rowland I, Wiseman H, Sanders T, Adlercreutz H & Bowey E (1999): Metabolism of oestrogens and phytoestrogens: role of the gut microflora. Biochem. Soc. Trans. 27, 304–308.

    Article  CAS  Google Scholar 

  • Rowland IR, Wiseman H, Sanders TA, Adlercreutz H & Bowey EA (2000): Interindividual variation in metabolism of soy isoflavones and lignans: influence of habitual diet on equol production by the gut microflora. Nutr. Cancer 36, 27–32.

    Article  CAS  Google Scholar 

  • Tsangalis D, Ashton JF, McGill AEJ & Shah NP (2003): Biotransformation of isoflavones by bifidobacteria in fermented soymilk supplemented with D-glucose and L-cysteine. J. Food Sci. 68, 623–631.

    Article  CAS  Google Scholar 

  • Volek JS, Kraemer WJ, Bush JA, Incledon T & Boetes M (1997): Testosterone and cortisol in relationship to dietary nutrients and resistance exercise. J. Appl. Physiol. 82, 49–54.

    Article  CAS  Google Scholar 

  • Wu AH, Ziegler RG, Horn-Ross PL, Nomura AM, West DW, Kolonel LN, Rosenthal JF, Hoover RN & Pike MC (1996): Tofu and risk of breast cancer in Asian-Americans. Cancer Epidemiol. Biomarkers Prev. 5, 901–906.

    CAS  PubMed  Google Scholar 

  • Zheng W, Dai Q, Custer LJ, Shu XO, Wen WQ, Jin F & Franke AA (1999): Urinary excretion of isoflavonoids and the risk of breast cancer. Cancer Epidemiol. Biomarkers Prev. 8, 35–40.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the General Clinical Research Center Grant MO1-RR00400 from the National Center for Research Resources and the Minnesota Agricultural Experiment Station. We would like to thank the study participants for their time and dedication, as well as the staff at the General Clinical Research Center, University of Minnesota. We are grateful to Jennifer Nettleton, Kris Greany, and Jill Hamilton-Reeves for their help with laboratory assays and Will Thomas for his help with statistical analysis. The soy protein isolate and probiotic capsules were generously donated by The Solae Company, St. Louis, MO, and UAS Laboratories, Minnetonka, MN, respectively.

Author information

Authors and Affiliations

  1. Department of Food Science and Nutrition, University of Minnesota, St. Paul, MN, USA

    M J L Bonorden, K A Greany, K E Wangen, J Feirtag & M S Kurzer

  2. Department of Obstetrics and Gynecology, University of Rochester, Rochester, NY, USA

    W R Phipps

  3. Division of Clinical Chemistry, University of Helsinki, Helsinki, Finland

    H Adlercreutz

Authors
  1. M J L Bonorden
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K A Greany
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K E Wangen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. W R Phipps
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J Feirtag
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H Adlercreutz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M S Kurzer
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Contributors: MJLB was the primary author and study coordinator and assisted with subject recruiting; KAG was a study co-coordinator and assisted with subject recruiting; KEW helped with study design; WRP assisted with study design and provided medical consulting; JF assisted with study design and provided microbiological consulting; HA developed and performed the equol analysis; MSK was the principal investigator, who supervised all aspects of the study. All authors contributed to the data interpretation and manuscript preparation.

Corresponding author

Correspondence to M S Kurzer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bonorden, M., Greany, K., Wangen, K. et al. Consumption of Lactobacillus acidophilus and Bifidobacterium longum do not alter urinary equol excretion and plasma reproductive hormones in premenopausal women. Eur J Clin Nutr 58, 1635–1642 (2004). https://doi.org/10.1038/sj.ejcn.1602020

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.ejcn.1602020

Keywords

This article is cited by

Search

Advanced search

Quick links