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Cited by 151Phytoestrogen effects and researchDigital Radiography and Breast ImagingEstrogen and related hormone effects

Red-clover-derived isoflavones and mammographic breast density: a double-blind, randomized, placebo-controlled trial [ISRCTN42940165

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Atkinson, Charlotte, Warren, Ruth ML, Sala, Evis, Dowsett, Mitch, Dunning, Alison M, Healey, Catherine S, Runswick, Shirley, Day, Nicholas E +1 more·2004·Breast Cancer Research
DOI 10.1186/bcr773PMC PMC400670
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Abstract

INTRODUCTION: Isoflavones are hypothesized to protect against breast cancer, but it is not clear whether they act as oestrogens or anti-oestrogens in breast tissue. Our aim was to determine the effects of taking a red clover-derived isoflavone supplement daily for 1 year on mammographic breast density. Effects on oestradiol, follicle-stimulating hormone (FSH), luteinizing hormone (LH), lymphocyte tyrosine kinase activity and menopausal symptoms were also assessed. METHODS: A total of 205 women (age range 49-65 years) with Wolfe P2 or DY mammographic breast patterns were randomly assigned to receive either a red clover-derived isoflavone tablet (26 mg biochanin A, 16 mg formononetin, 1 mg genistein and 0.5 mg daidzein) or placebo. Change in mammographic breast density, serum oestradiol, FSH, LH, menopausal symptoms and lymphocyte tyrosine kinase activity from baseline to 12 months were assessed. RESULTS: A total of 177 women completed the trial. Mammographic breast density decreased in both groups but the difference between the treatment and placebo was not statistically significant. There was a significant interaction between treatment group and oestrogen receptor (ESR1) PvuII polymorphism for the change in estimated percentage breast density (mean +/- standard deviation): TT isoflavone 1.4 +/- 12.3% and TT placebo -9.6 +/- 14.2%; CT isoflavone -5.2 +/- 12.0% and CT placebo -2.8 +/- 10.3%; and CC isoflavone -3.4 +/- 9.7% and CC placebo -1.1 +/- 9.5%. There were no statistically significant treatment effects on oestradiol, FSH, or LH (assessed only in postmenopausal women), or on lymphocyte tyrosine kinase activity. Baseline levels of menopausal symptoms were low, and there were no statistically significant treatment effects on frequency of hot flushes or other menopausal symptoms. CONCLUSION: In contrast to studies showing that conventional hormone replacement therapies increase mammographic breast density, the isoflavone supplement did not increase mammographic breast density in this population of women. Furthermore, there were no effects on oestradiol, gonadotrophins, lymphocyte tyrosine kinase activity, or menopausal symptoms.

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  • The Atkinson trial was assessed as having low risk of bias in approximately half of the categories but failed to provide adequate information to assess selection bias, detection bias, and attrition bias.

    “The trial by Atkinson was assessed as having low risk of bias in approximately half of the categories but failed to provide adequate information to assess for selection bias, detection bias, and attrition bias [165].”

    From Soy, Red Clover, and Isoflavones and Breast Cancer: A Systematic Review (2013) · cites this paper as [165]

    The Methods (Intervention and randomization; Mammographic density) describe random-number generation, who handled randomization, and blinding of researchers, participants, and radiologists. The Results (Withdrawals and baseline data) give the number and reasons for withdrawals and compare withdrawals between groups. The paper does not make the cited risk-of-bias assessment, and its reporting runs contrary to the claim that it lacked adequate information on detection and attrition bias. (LLM, conf=0.78)

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  • Atkinson reported no significant change in estradiol over one year: estradiol increased by 14.0 pmol/L in the red clover group compared with a decrease of 0.9 in the placebo group, p=0.49.

    “Atkinson reported no significant changes in estradiol, FSH, or LH over the one year period: estradiol increased by 14.0 pmol/L in the red clover group compared to a decrease of 0.9 in the placebo group, however this was not significant, p=0.49);”

    From Soy, Red Clover, and Isoflavones and Breast Cancer: A Systematic Review (2013) · cites this paper as [165]

    The Results section reports no significant treatment-group effect on changes in oestradiol, FSH, or LH from baseline to 12 months. The quoted estradiol changes of +14.0 and −0.9 pmol/L and p=0.49 are not present in the available passages, so those figures cannot be verified from our copy. The Methods specify that hormone changes were assessed only in postmenopausal women. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

  • Atkinson reported no significant change in FSH: FSH decreased 4.2 IU/L in the red clover group compared with a decrease of 2.9 in the placebo group, p=0.83.

    “FSH decreased 4.2 IU/L in the red clover group compared to a decrease of 2.9 in the placebo group, p=0.83;”

    From Soy, Red Clover, and Isoflavones and Breast Cancer: A Systematic Review (2013) · cites this paper as [165]

    The Results section on oestradiol and gonadotrophins states that treatment group had no significant effect on change in FSH. Our copy does not provide the claimed overall decreases of 4.2 and 2.9 IU/L or P = 0.83; the Results refer to Table 2 but give only genotype-specific FSH changes in the available passage. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • Atkinson's RCT showed no significant changes in hot flash score (p=0.88) or mean number of daily hot flashes (p=0.41) when groups were compared.

    “Results of the study by Atkinson showed no significant changes in hot flash score (p=0.88) or mean number of daily hot flashes (p=0.41) when groups were compared [165].”

    From Soy, Red Clover, and Isoflavones and Breast Cancer: A Systematic Review (2013) · cites this paper as [165]

    The Results section, “Hot flushes and menopausal symptoms” (page unavailable), reports no significant treatment-group effect on the number of hot flushes or the menopausal symptom score. It does not give the claimed p-values of 0.41 and 0.88 for those outcomes; the Methods section describes the score as covering 21 menopausal symptoms, not hot flashes alone. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Atkinson reported no significant change in LH: LH decreased 4.0 IU/L in the red clover group compared with a decrease of 4.2 IU/L in the placebo group, p=0.71.

    “LH decreased 4.0 IU/L in the red clover group compared to a decrease of 4.2 IU/L in the placebo group, p=0.71;”

    From Soy, Red Clover, and Isoflavones and Breast Cancer: A Systematic Review (2013) · cites this paper as [165]

    The Results section on luteinizing hormone reports no significant treatment-group effect on the change in LH. Our copy does not give the claimed decreases of 4.0 and 4.2 IU/L or P = 0.71; the Results refer to Table 2, but those figures are not present in the available passages. The Methods section says LH changes were assessed only in postmenopausal women. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

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Cited by

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Authors
Atkinson, C., Warren, R. M., Sala, E., Dowsett, M., Dunning, A. M., Healey, C. S., Runswick, S., Day, N. E., & Bingham, S. A.
Affiliations
  • MRC Biostatistics Unit (GB)
  • Addenbrooke's Hospital (GB)
  • Royal Marsden Hospital (GB)
  • MRC Mitochondrial Biology Unit (GB)
Corresponding author
Bingham, Sheila A
ORCID
Venue
Breast Cancer Research
Publisher
Springer Science and Business Media LLC
Published
2004-02-24
Volume
6
Issue
3
Pages
R170-9
ISSN
  • 1465-5411 (ISSN-L)
  • 1465-542X
DOI
10.1186/bcr773
PMC
PMC400670
OpenAlex
W1586711992
Cited by
151
References
0
Citations by year
2026: 2 · 2025: 2 · 2024: 4 · 2023: 2 · 2022: 2 · 2021: 2 · 2020: 2 · 2019: 3 · 2017: 1 · 2016: 8 · 2015: 7 · 2014: 4 · 2013: 5 · 2012: 8
FWCI
11.46
Type
journal article
Language
en
Open access
Licence
Locations
  • Breast Cancer Research (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, other-oa)
  • Explore Bristol Research (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Food Standards Agency
  • Medical Research Council
Topics
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Phytoestrogen effects and research
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Digital Radiography and Breast Imaging
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Keywords
isoflavones, red clover, breast density, biochanin A, formononetin, genistein, daidzein, PvuII polymorphism, estradiol, follicle-stimulating hormone, luteinizing hormone, menopausal symptoms, hot flashes, postmenopausal women, breast cancer prevention, phytoestrogens, hormone replacement therapy
MeSH terms
Adipose Tissue, Aged, Breast, Connective Tissue, Double-Blind Method, Estradiol, Female, Follicle Stimulating Hormone, Humans, Isoflavones, Luteinizing Hormone, Lymphocytes, Mammography, Menopause, Middle Aged, Plant Extracts, Protein-Tyrosine Kinases, Biomarkers, Anticarcinogenic Agents, Hot Flashes, Genistein, Trifolium

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