The DOI matches its Crossref record; 35 of the 35 references it cites were found in a registry or an index.
The Impact of Macronutrient Intake on Sex Steroids During Onset of Puberty
Open accessAbstract
Introduction Increased fiber intake has been associated with decreased breast cancer risk, while increased animal protein intake with increased risk. The objective of this study is to examine the relationship of dietary fiber and protein intake to estrogen and sex hormone-binding globulin (SHBG) concentrations at puberty onset. Methods These analyses were conducted using the Cincinnati puberty cohort of the Breast Cancer and the Environment Research Program, with girls followed every 6 months from ages 6 and 7. The analyses included serum measurements at 6-month intervals for estrogen and SHBG concentrations, from 18 months prior to breast stage 2 (onset of puberty). Dietary intake was documented via 24-hour dietary recalls every 3 months. Dietary factors of interest included total energy intake; total and animal protein; total, soluble, and insoluble fiber; and lignan and flavanol intake. Results This study included 260 participants who generated 871 serum specimens and 3,000 days of diet intake. In longitudinal models, estradiol was associated inversely with insoluble fiber intake; estrone positively with animal protein intake; SHBG with greater insoluble fiber and lower total protein intake; and ratio of estrone to SHBG, a measure of bioavailable estrogen, positively with animal protein. Conclusions Greater protein intake, especially animal protein, led to greater estrogen concentrations and lower SHBG; greater animal protein and greater caloric intake led to increased bioavailable estrogen. This relationship may have served an evolutionary advantage in the past for greater fertility with adequate high-quality protein; in contemporary women, a modest decrease in animal protein may be beneficial in reducing breast cancer risk.
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“Biro et al. (2022) also stated that females with higher fiber consumption had markedly higher testosterone levels; thus, they further confirmed that the hormonal effects are directly related to fiber intake [124].”
From Nutritional and herbal interventions for polycystic ovary syndrome (PCOS): a comprehensive review of dietary approaches, macronutrient impact, and herbal medicine in management (2025) · cites this paper as Biro et al. (2022)
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“Biro et al. (2022) also stated that females with higher fiber consumption had markedly higher testosterone levels; thus, they further confirmed that the hormonal effects are directly related to fiber intake [124].”
From Nutritional and herbal interventions for polycystic ovary syndrome (PCOS): a comprehensive review of dietary approaches, macronutrient impact, and herbal medicine in management (2025) · cites this paper as [124]
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ANDERSON, D. C. (1974) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1974.tb03298.x · Cited by 1,127
Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens
Adlercreutz, H., Bannwart, C., Wähälä, K., Mäkelä, T., Brunow, G., Hase, T. A., Arosemena, P. J., Kellis, J. T., & Vickery, L. E. (1993) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(93)90022-o · Cited by 544
Estrogen excretion patterns and plasma levels in vegetarian and omnivorous women
Goldin, B. R., Adlercreutz, H., Gorbach, S. L., Warram, J. H., Dwyer, J. T., Swenson, L., & Woods, M. N. (1982) · New England Journal of Medicine · doi:10.1056/nejm198212163072502 · Cited by 474
Pubertal assessment method and baseline characteristics in a mixed longitudinal study of girls
Biro, F. M., Galvez, M. P., Greenspan, L. C., Succop, P. A., Vangeepuram, N., Pinney, S. M., Teitelbaum, S., Windham, G. C., Kushi, L. H., & Wolff, M. S. (2010) · Pediatrics · doi:10.1542/peds.2009-3079 · Cited by 348
Self-citationDietary fiber intake and risk of type 2 diabetes: a dose–response analysis of prospective studies
Yao, B., Fang, H., Xu, W., Yan, Y., Xu, H., Liu, Y., Mo, M., Zhang, H., & Zhao, Y. (2014) · European Journal of Epidemiology · doi:10.1007/s10654-013-9876-x · Cited by 281
Relation of Childhood Diet and Body Size to Menarche and Adolescent Growth in Girls
Berkey, C. S. (2000) · American Journal of Epidemiology · doi:10.1093/aje/152.5.446 · Cited by 247
Dietary fiber and breast cancer risk: a systematic review and meta-analysis of prospective studies
Aune, D., Chan, D. S. M., Greenwood, D. C., Vieira, A., Navarro-Rosenblatt, D., Vieira, R. D. C. P. A., & Norat, T. (2012) · Annals of Oncology · doi:10.1093/annonc/mdr589 · Cited by 241
Assessing Phytoestrogen Exposure in Epidemiologic Studies: Development of a Database (United States)
Horn‐Ross, P. L., Barnes, S., Lee, M., Coward, L. U., Mandel, J. E., Koo, J., John, E. M., & Smith, M. (2000) · Cancer Causes & Control · doi:10.1023/a:1008995606699 · Cited by 240
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High intakes of skimmed milk, but not meat, increase serum IGF-I and IGFBP-3 in eight-year-old boys
Hoppe, C., Mølgaard, C., Juul, A., & Michaelsen, K. F. (2004) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601948 · Cited by 221
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Muhammed Saeed, A. A., Noreen, S., Awlqadr, F. H., Farooq, M. I., Qadeer, M., Rai, N., Farag, H. A., & Saeed, M. N. (2025) · Journal of Health, Population and Nutrition · doi:10.1186/s41043-025-00899-y · Cited by 29
“Biro et al. (2022) also stated that females with higher fiber consumption had markedly higher testosterone levels; thus, they further confirmed that the hormonal effects are directly related to fiber intake [124].”
Association of the consumption of common drinks with early puberty in both sexes
Tsai, M., Lee, Y. L., & Chen, Y. (2022) · Frontiers in Public Health · doi:10.3389/fpubh.2022.854477 · Cited by 11
Hayta, Ü., Dinç, N., & Taneli, F. (2024) · HORMONES · doi:10.1007/s42000-024-00591-6 · Cited by 2
The Influence of Diet on Cancer Progression and Treatment
Barbeau, A. M., Kincaid, J. W. R., Hillis, A. L., Rashan, E. H., Zhang, Y., Oaks, G. E., & Heiden, M. G. V. (2026) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-062122-021518 · Cited by 3
Zhang, Z., Liu, Y., Zhao, J., Chen, W., & Wang, G. (2025) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2025.105416
Metadata
- Authors
- Biro, F. M., Summer, S. S., Huang, B., Chen, C., Benoit, J., & Pinney, S. M.
- Affiliations
- Cincinnati Children's Hospital Medical Center (US)
- University of Cincinnati (US)
- Corresponding author
- Biro, Frank M.
- Venue
- Journal of Adolescent Health
- Publisher
- Elsevier BV
- Published
- 2022-03
- Volume
- 70
- Issue
- 3
- Pages
- 483-487
- ISSN
- 1054-139X (ISSN-L)
- PMC
- PMC8860866
- OpenAlex
- W3216064545
- Cited by
- 6
- References
- 35
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2022: 1
- FWCI
- 0.43
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Adolescent Health (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH
- National Cancer Institute
- National Institute of Environmental Health Sciences (R01 ES029133, UL1 RR026314)
- U.S. Public Health Service (8 UL1 TR000077–05, P30 ES006096)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Health Sciences › Medicine › Oncology › Cancer Risks and Factors
- Health Sciences › Nursing › Nutrition and Dietetics › Phytoestrogen effects and research
- Keywords
- dietary fiber, animal protein intake, macronutrients, puberty onset, sex hormones, estradiol, estrone, sex hormone-binding globulin, lignans, flavonoids, breast cancer risk, adolescent girls
- MeSH terms
- Child, Eating, Estradiol, Estrogens, Female, Humans, Puberty, Gonadal Steroid Hormones
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