Effects of Dietary Phytoestrogens on Hormones Throughout A
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nutrients Review Effects of Dietary Phytoestrogens on Hormones throughout a Human Lifespan: A Review Inés Domínguez-López 1 , Maria Yago-Aragón 1, Albert Salas-Huetos 2 , Anna Tresserra-Rimbau 1,3,4,5,* and Sara Hurtado-Barroso 1,3 1 Department of Nutrition, Food Science and Gastronomy, XaRTA, INSA, School of Pharmacy and Food Sciences, University of Barcelona, 08028 Barcelona, Spain; [email protected] (I.D.-L.); [email protected] (M.Y.-A.); [email protected] (S.H.-B.) 2 Andrology and IVF Laboratory, Division of Urology, Department of Surgery, University of Utah School of Medicine, Salt Lake City, UT 84108, USA; [email protected] 3 Centro de Investigación Biomédica en Red Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029 Madrid, Spain 4 Unitat de Nutrició, Departament de Bioquímica i Biotecnologia, Universitat Rovira i Virgili, 43204 Reus, Spain 5 Institut d’Investigació Sanitària Pere Virgili (IISPV), 43201 Reus, Spain * Correspondence: [email protected] Received: 7 July 2020; Accepted: 12 August 2020; Published: 15 August 2020 Abstract: Dietary phytoestrogens are bioactive compounds with estrogenic activity. With the growing popularity of plant-based diets, the intake of phytoestrogen-rich legumes (especially soy) and legume-derived foods has increased. Evidence from preclinical studies suggests these compounds may have an effect on hormones and health, although the results of human trials are unclear. The effects of dietary phytoestrogens depend on the exposure (phytoestrogen type, matrix, concentration, and bioavailability), ethnicity, hormone levels (related to age, sex, and physiological condition), and health status of the consumer. In this review, we have summarized the results of human studies on dietary phytoestrogens with the aim of assessing the possible hormone-dependent outcomes and health effects of their consumption throughout a lifespan, focusing on pregnancy, childhood, adulthood, and the premenopausal and postmenopausal stages. In pregnant women, an improvement of insulin metabolism has been reported in only one study. Sex hormone alterations have been found in the late stages of childhood, and goitrogenic effects in children with hypothyroidism. In premenopausal and postmenopausal women, the reported impacts on hormones are inconsistent, although beneficial goitrogenic effects and improved glycemic control and cardiovascular risk markers have been described in postmenopausal individuals. In adult men, different authors report goitrogenic effects and a reduction of insulin in non-alcoholic fatty liver patients. Further carefully designed studies are warranted to better elucidate the impact of phytoestrogen consumption on the endocrine system at different life stages. Keywords: isoflavones; soy; dietary flavonoids; lignans; flaxseeds; endocrine; stages of life; estrogenic; polyphenols; health 1. Introduction Phytoestrogens are polyphenolic molecules with a structural similarity to endogenous human hormones, hence their estrogenic activity. The main dietary source of these plant secondary metabolites is legumes (particularly soy), and to a lesser extent fruits, vegetables, and cereals [1]. Figure1 shows the most common phytoestrogens in diet. According to their origin, lignins are classified into plant lignans (e.g., pinoresinol, secoisolariciresinol, matairesinol, and sesamin) and enterolignans (e.g., enterodiol Nutrients 2020, 12, 2456; doi:10.3390/nu12082456 www.mdpi.com/journal/nutrients Nutrients 2020, 12, 2456 2 of 25 Nutrients 2020, 12, x FOR PEER REVIEW 2 of 25 andintestinal enterolactone), bacteria [1]. which Although are metabolized ingested from in lower plant lignansquantities by intestinalthan isoflavones bacteria [1and]. Although lignans, ingestedprenylflavonoids in lower quantitiesfrom beer than and isoflavones coumestans and from lignans, soy prenylflavonoids are also regarded from as beer polyphenols and coumestans with fromestrogenic soy are activity. also regarded as polyphenols with estrogenic activity. Figure 1. Classification and examples of the most common dietary phytoestrogens. Images are the chemicalFigure 1. structuresClassification of genistein, and examples coumestrol, of the andmost enterodiol. common dietary phytoestrogens. Images are the chemical structures of genistein, coumestrol, and enterodiol. The intake of phytoestrogens has increased due to the widespread use of soy products for human consumptionThe intake and of asphytoestrogens cattle food [2 ].has In increased Europe, the due lowest to the averagewidespread intake use of of phytoestrogens soy products for occurs human in Mediterraneanconsumption and countries, as cattle whereas food [2]. consumption In Europe, the in Northernlowest average countries intake is 0.76of phytoestrogens mg/day [3]. The occurs highest in soy-derivedMediterranean isoflavone countries, intakes whereas worldwide consumption are still in in Nort Chinahern and countries Japan, where is 0.76 the mg/day population [3]. The consumes highest ansoy-derived average of isoflavone 15–50 mg intakes per day, worldwide compared toare only still about in China 2 mg and per dayJapan, in Westernwhere the countries population [4,5]. Theconsumes promising an average health of eff 15–50ects of mg soy per have day, driven compared some to people only about in developed 2 mg per countries day in Western to consume countries it as an[4,5]. alternative The promising to meat health or dairy effects products. of soy have driven some people in developed countries to consume it as anDietary alternative phytoestrogens to meat or aredairy digested products. in the small intestine, where they are poorly absorbed. ThoseDietary that reach phytoestrogens the liver are conjugatedare digested and in circulate the smal inl theintestine, plasma where until excretion they arein poorly urine. absorbed. Thos that areThose not that absorbed reach arethe metabolized liver are conjugated by the gut and microbiota circulate into in lowerthe plasma weight until compounds excretion [1 in]. Theurine. diversity Those ofthat food are matricesnot absorbed (from are pure metabolized compounds by to the complex gut microbiota foods) used into in lower clinical weight studies compounds could also [1]. lead The to didiversityfferent results of food although matrices interindividual (from pure compounds variability seems to complex more determinant. foods) used Itin has clinical been demonstratedstudies could thatalso phytoestrogenlead to different extraction results although from complex interindividual food matrices, variability such seems as those more with determinant. high content It ofhas sugars been anddemonstrated proteins, is that more phytoestrogen difficult in in vitroextractionstudies; from however, complex no clearfood dimatrices,fferences such regarding as those food with matrices high werecontent observed of sugars in humansand proteins, [6]. Nevertheless, is more difficult results in in using vitro pure studies; compounds however, must no clear be extrapolated differences carefullyregarding because food matrices not only were is observed the matrix in dihumansfferent, [6]. but Nevertheless, also the concentration, results using which pure iscompounds higher in puremust extracts.be extrapolated carefully because not only is the matrix different, but also the concentration, whichResults is higher from in humanpure extracts. studies suggest that phytoestrogens may lower the risk of osteoporosis, someResults cardiometabolic from human diseases, studies cognitive suggest dysfunction,that phytoestrogens breast and may prostate lower cancer,the risk and of osteoporosis, menopausal symptomssome cardiometabolic by modulating diseases, the endocrine cognitive system dysfunctio (Figure2).n, However, breast and some prostate authors cancer, describe and phytoestrogens menopausal assymptoms endocrine by disruptors modulating and believe the endocrine their beneficial system effects (Figure have been 2). overestimatedHowever, some[2,5 ,7authors]. This ambiguity describe couldphytoestrogens be partially as dueendocrine to the disruptors variability and of published believe their studies, beneficial as the effects beneficial have or been harmful overestimated effects of phytoestrogens[2,5,7]. This ambiguity depend could on the be partially exposure due (type, to the amount variability consumed, of published and bioavailability), studies, as the beneficial ethnicity, hormonalor harmful status effects (age of and phytoestrogens sex and physiological depend condition), on the exposure and health (type, status amount of the consumerconsumed, [2 ,5and,7]. bioavailability), ethnicity, hormonal status (age and sex and physiological condition), and health status of the consumer [2,5,7]. Nutrients 2020, 12, 2456 3 of 25 Nutrients 2020, 12, x FOR PEER REVIEW 3 of 25 FigureFigure 2.2. Summary of potentialpotential healthhealth outcomesoutcomes ofof phytoestrogensphytoestrogens through thethe modulationmodulation ofof thethe endocrineendocrine systemsystem inin ((aa)) thyroids,thyroids, ((bb)) liver,liver, ((cc)) ovaries,ovaries, ((dd)) bones,bones, ((ee)) hypothalamic–pituitary–gonadalhypothalamic–pituitary–gonadal axis,axis, ((ff)) pancreas,pancreas, ((gg)) fatfat tissue, (h) prostate. FSH: FSH: follicle-stimulating follicle-stimulating hormone; hormone; GnRH: GnRH: gonadotropin- gonadotropin- releasingreleasing hormone; IGF-1: IGF-1: insulin insulin growth growth factor factor 1; 1;LH: LH: luteinizing luteinizing hormone; hormone; OC: OC:osteocalcin;