Cited by 68

The DOI matches its Crossref record; 8 of the 8 references it cites were found in a registry or an index.

Association between Dietary Share of Ultra-Processed Foods and Urinary Concentrations of Phytoestrogens in the US

Martínez Steele, Eurídice, Monteiro, Carlos·2017·Nutrients

Abstract

The aim of this study was to examine the relationship between dietary contribution of ultra-processed foods and urinary phytoestrogen concentrations in the US. Participants from cross-sectional 2009–2010 National Health and Nutrition Examination Survey aged 6+ years, selected to measure urinary phytoestrogens and with one 24-h dietary recall were evaluated (2692 participants). Food items were classified according to NOVA (a name, not an acronym), a four-group food classification based on the extent and purpose of industrial food processing. Ultra-processed foods are formulations manufactured using several ingredients and a series of processes (hence “ultra-processed”). Most of their ingredients are lower-cost industrial sources of dietary energy and nutrients, with additives used for the purpose of imitating sensorial qualities of minimally processed foods or of culinary preparations of these foods. Studied phytoestrogens included lignans (enterolactone and enterodiol) and isoflavones (genistein, daidzein, O-desmethylangolensin and equol). Gaussian regression was used to compare average urinary phytoestrogen concentrations (normalized by creatinine) across quintiles of energy share of ultra-processed foods. Models incorporated survey sample weights and were adjusted for age, sex, race/ethnicity, family income, and education, among other factors. Adjusted enterodiol geometric means decreased monotonically from 60.6 in the lowest quintile to 35.1 µg/g creatinine in the highest, while adjusted enterolactone geometric means dropped from 281.1 to 200.1 across the same quintiles, respectively. No significant linear trend was observed in the association between these quintiles and isoflavone concentrations. This finding reinforces the existing evidence regarding the negative impact of ultra-processed food consumption on the overall quality of the diet and expands it to include non-nutrients such as lignans.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/nu9030209

Cites

8 of 8 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Nationally representative US studies found linear inverse associations between UPF quintiles and flavonoid intake, and urinary concentrations of phytoestrogens.

    “Furthermore, nationally representative US studies found linear inverse associations between UPF quintiles and flavonoid intake, 66 and urinary concentrations of phytoestrogens.67”

    From Ultra-processed foods and human health: the main thesis and the evidence (2025) · cites this paper as [67]

    Methods §2.1 identifies the data as nationally representative US NHANES data. Results §3.2 reports an inverse linear trend across UPF-share quintiles for urinary enterodiol and enterolactone, but no significant linear trend for the four urinary isoflavones. Thus, the citation supports the urinary-concentration part of the sentence only for some phytoestrogens; the flavonoid-intake finding is attached to a different citation. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

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

Flagged first, then by citations

Research works printed but not linked: 51

  1. Paterni, I., Granchi, C., and Minutolo, F. (2016). Risks and Benefits Related to Alimentary Exposure to Xenoestrogens. Crit. Rev. Food Sci. Nutr. · DOI
  2. Wang, 2002, Mammalian phytoestrogens: Enterodiol and enterolactone, J. Chromatogr. B, 777, 289, 10.1016/S1570-0232(02)00281-7 · DOI
  3. Sirotkin, 2014, Phytoestrogens and their effects, Eur. J. Pharmacol., 741, 230, 10.1016/j.ejphar.2014.07.057 · DOI
  4. Cassidy, 2003, Potential risks and benefits of phytoestrogen-rich diets, Int. J. Vitam. Nutr. Res., 73, 120, 10.1024/0300-9831.73.2.120 · DOI
  5. Tuohy, 2003, Soy infant formula and phytoestrogens, J. Paediatr. Child Health, 39, 401, 10.1046/j.1440-1754.2003.00178.x · DOI
  6. Branca, 2005, Health effects of phytoestrogens, Forum Nutr., 57, 100, 10.1159/000083773 · DOI
  7. Vitale, 2013, Isoflavones: Estrogenic activity, biological effect and bioavailability, Eur. J. Drug Metab. Pharmacokinet., 38, 15, 10.1007/s13318-012-0112-y · DOI
  8. Grace, 2004, Phytoestrogen Concentrations in Serum and Spot Urine as Biomarkers for Dietary Phytoestrogen Intake and Their Relation to Breast Cancer Risk in European Prospective Investigation of Cancer and Nutrition-Norfolk, Cancer Epidemiol. Biomark. Prev., 13, 698, 10.1158/1055-9965.698.13.5 · DOI · Paper page
  9. Eldrige, 1983, Soybean isoflavones: Effect of environment and variety on composition, J. Agric. Food Chem., 31, 394, 10.1021/jf00116a052 · DOI
  10. Wang, 1994, Isoflavone composition of American and Japanese soybeans in Iowa: Effects of variety, crop year and location, J. Agric. Food Chem., 42, 1674, 10.1021/jf00044a017 · DOI
  11. Wang, 1994, Isoflavone content in commercial soybean foods, J. Agric. Food Chem., 42, 1666, 10.1021/jf00044a016 · DOI
  12. Thompson, 1997, Variability in anticancer lignan levels in flaxseed, Nutr. Cancer, 27, 26, 10.1080/01635589709514497 · DOI
  13. Setchell, 2003, Variations in isoflavone levels in soy foods and soy protein isolates and issues related to isoflavone databases and food labeling, J. Agric. Food Chem., 51, 4146, 10.1021/jf026199b · DOI
  14. Lampe, 2003, Isoflavonoid and lignan phytoestrogens as dietary biomarkers, J. Nutr., 133, 956S, 10.1093/jn/133.3.956S · DOI
  15. Seow, 1998, Isoflavonoid levels in spot urine are associated with frequency of dietary soy intake in a population-based sample of middle aged and older Chinese in Singapore, Cancer Epidemiol. Biomark. Prev., 7, 135
  16. French, 2007, Validation of a phytoestrogen food frequency questionnaire with urinary concentrations of isoflavones and lignan metabolites in premenopausal women, J. Am. Coll. Nutr., 26, 76, 10.1080/07315724.2007.10719588 · DOI
  17. Maskarinec, 1998, Dietary soy intake and urinary isoflavone excretion among women from a multiethnic population, Cancer Epidemiol. Biomark. Prev., 7, 613
  18. Fraser, 2008, Validation of soy protein estimates from a food-frequency questionnaire with repeated 24-h recalls and isoflavonoid excretion in overnight urine in a western population with a wide range of soy intakes, Am. J. Clin. Nutr., 87, 1422, 10.1093/ajcn/87.5.1422 · DOI
  19. Lampe, 1999, Urinary isoflavonoid and lignan excretion on a western diet: Relation to soy, vegetable, and fruit intake, Cancer Epidemiol. Biomark. Prev., 8, 699
  20. Monteiro, 2009, Nutrition and health. The issue is not food, nor nutrients, so much as processing, Public Health Nutr., 12, 729, 10.1017/S1368980009005291 · DOI
  21. Ludwig, 2011, Technology, diet, and the burden of chronic disease, JAMA, 305, 1352, 10.1001/jama.2011.380 · DOI
  22. Neff, R. (2015). Introduction to U.S. Food System. Public Health, Environment, and Equity, Jossey Bass A Wiley Brand.
  23. Monteiro, 2013, Ultra-processed products are becoming dominant in the global food system, Obes. Rev., 14, 21, 10.1111/obr.12107 · DOI · Paper page
  24. Pimenta, 2016, Ultraprocessed food consumption and risk of overweight and obesity: The University of Navarra Follow-Up (SUN) cohort study, Am. J. Clin. Nutr., 104, 1433, 10.3945/ajcn.116.135004 · DOI · Paper page
  25. Rauber, 2015, Consumption of ultra-processed food products and its effects on children’s lipid profiles: A longitudinal study, Nutr. Metab. Cardiovasc. Dis., 25, 116, 10.1016/j.numecd.2014.08.001 · DOI
  26. Baraldi, 2016, Ultra-processed foods and added sugars in the US diet: Evidence from a nationally representative cross-sectional study, BMJ Open, 6, e009892, 10.1136/bmjopen-2015-009892 · DOI · Paper page
  27. Monteiro, 2010, Increasing consumption of ultra-processed foods and likely impact on human health: Evidence from Brazil, Public Health Nutr., 14, 5, 10.1017/S1368980010003241 · DOI · Paper page
  28. Louzada, M.L., Martins, A.P., Canella, D.S., Baraldi, L.G., Bertazzi, R.L., Claro, R.M., Moubarac, J.C., Cannon, G., and Monteiro, C.A. (2015). Ultra-processed foods and the nutritional dietary profile in Brazil. Rev. Saúde Pública, 49. · DOI
  29. Louzada, M.L., Martins, A.P., Canella, D.S., Baraldi, L.G., Bertazzi, R.L., Claro, R.M., Moubarac, J.C., Cannon, G., and Monteiro, C.A. (2015). Impact of ultra-processed foods on micronutrient content in the Brazilian diet. Rev. Saúde Pública, 49. · DOI
  30. Moubarac, 2012, Consumption of ultra-processed foods and likely impact on human health. Evidence from Canada, Public Health Nutr., 16, 1
  31. Moshfegh, 2008, The USDA Automated Multiple-Pass Method reduces bias in the collection of energy intakes, Am. J. Clin. Nutr., 88, 324, 10.1093/ajcn/88.2.324 · DOI
  32. Blanton, 2006, The USDA Automated Multiple-Pass Method accurately estimates group total energy and nutrient intake, J. Nutr., 136, 2594, 10.1093/jn/136.10.2594 · DOI
  33. Rumpler, 2008, Identifying sources of reporting error using measured food intake, Eur. J. Clin. Nutr., 62, 544, 10.1038/sj.ejcn.1602742 · DOI
  34. Lyles, 2001, Correlation coefficient estimation involving a left censored laboratory assay variable, Statist. Med., 20, 2921, 10.1002/sim.901 · DOI
  35. Monteiro, 2010, A new classification of foods based on the extent and purpose of their processing, Cad. Saúde Pública, 26, 2039, 10.1590/S0102-311X2010001100005 · DOI · Paper page
  36. Moubarac, 2014, Food Classification Systems Based on Food Processing: Significance and implications for policies and actions: A systematic literature review and assessment, Curr. Obes. Rep., 3, 256, 10.1007/s13679-014-0092-0 · DOI · Paper page
  37. Monteiro, 2012, The Food System. Processing. The big issue for disease, good health, well-being, World Nutr., 3, 527
  38. Ahuja, J.K.A., Montville, J.B., Omolewa-Tomobi, G., Heendeniya, K.Y., Martin, C.L., Steinfeldt, L.C., Anand, J., Adler, M.E., LaComb, R.P., and Moshfegh, A.J. (2012). USDA Food and Nutrient Database for Dietary Studies, 5.0. · DOI
  39. Barnes, 2010, The biochemistry, chemistry and physiology of the isoflavones in soybeans and their food products, Lymphat. Res. Biol., 8, 89, 10.1089/lrb.2009.0030 · DOI
  40. Blount, 2003, Urinary and serum concentrations of seven phytoestrogens in a human reference population subset, J. Expo. Anal. Environ. Epidemiol., 13, 276, 10.1038/sj.jea.7500278 · DOI
  41. Clavel, 2006, Bioavailability of lignans in human subjects, Nutr. Res. Rev., 19, 187, 10.1017/S0954422407249704 · DOI
  42. Xu, 2015, Urinary enterolactone associated with liver enzyme levels in US adults: National Health and Nutrition Examination Survey (NHANES), Br. J. Nutr., 114, 91, 10.1017/S000711451500149X · DOI
  43. Xu, 2015, Urinary enterolactone is associated with obesity and metabolic alteration in men in the US National Health and Nutrition Examination Survey 2001–10, Br. J. Nutr., 113, 683, 10.1017/S0007114514004115 · DOI
  44. Reger, 2016, Urinary phytoestrogens and cancer, cardiovascular, and all‑cause mortality in the continuous National Health and Nutrition Examination Survey, Eur. J. Nutr., 55, 1029, 10.1007/s00394-015-0917-y · DOI
  45. Rowland, 2003, Bioavailability of phyto-oestrogens, Br. J. Nutr., 89, S45, 10.1079/BJN2002796 · DOI
  46. Subar, 2015, Addressing Current Criticism Regarding the Value of Self-Report Dietary Data, J. Nutr., 145, 2639, 10.3945/jn.115.219634 · DOI · Paper page
  47. Bingham, 2007, Epidemiologic assessment of sugars consumption using biomarkers: Comparisons of obese and nonobese individuals in the European Prospective Investigation of Cancer Norfolk, Cancer Epidemiol. Biomark. Prev., 16, 1651, 10.1158/1055-9965.EPI-06-1050 · DOI · Paper page
  48. Lafay, 2000, Does energy intake underreporting involve all kinds of food or only specific food items? Results from the Fleurbaix Laventie Ville Sante (FLVS) study, Int. J. Obes. Relat. Metab. Disord., 24, 1500, 10.1038/sj.ijo.0801392 · DOI
  49. Pryer, 1997, Who are the “low energy reporters” in the dietary and nutritional survey of British adults?, Int. J. Epidemiol., 26, 146, 10.1093/ije/26.1.146 · DOI
  50. Slining, 2015, An Approach to Monitor Food and Nutrition from “Factory to Fork”, J. Acad. Nutr. Diet., 115, 40, 10.1016/j.jand.2014.09.002 · DOI
  51. Setchell, 2003, Bioavailability, disposition, and dose-response effects of soy isoflavones when consumed by healthy women at physiologically typical dietary intakes, J. Nutr., 133, 1027, 10.1093/jn/133.4.1027 · DOI

Cited by

Sorted by citations

Metadata

Authors
Martínez Steele, E., & Monteiro, C.
Affiliations
Department of Nutrition, School of Public Health, University of São Paulo, São Paulo 01246-907, Brazil
Venue
Nutrients
Publisher
MDPI AG
Published
2017-02-28
Volume
9
Issue
3
Pages
209
ISSN
2072-6643
Cited by
68
References
8
Language
en
Funders
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico, Edital MCTI/CNPq/Universal (CNPq nº 443477/2014-0)
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP nº 2015/14900-9)

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