animals Review Impact of Estrogens Present in Environment on Health and Welfare of Animals Konrad Wojnarowski 1,* , Paweł Podobi ´nski 1, Paulina Cholewi ´nska 1 , Jakub Smoli ´nski 1 and Karolina Dorobisz 2 1 Institute of Animal Breeding, Wroclaw University of Environmental and Life Sciences, 51-630 Wroclaw, Poland; [email protected] (P.P.); [email protected] (P.C.); [email protected] (J.S.) 2 Department of Otolaryngology, Head and Neck Surgery, Wrocław Medical University, 50-556 Wrocław, Poland; [email protected] * Correspondence: [email protected] Simple Summary: Estrogens are a group of steroid hormones that recently have gained even more attention in the eyes of scientists. There is an ongoing discussion in the scientific community about their relevance as environmental contaminants and the danger they pose to animal health and welfare. In available literature we can find many examples of their negative effects and mechanisms that are involved with such phenomena. Abstract: Nowadays, there is a growing interest in environmental pollution; however, knowledge about this aspect is growing at an insufficient pace. There are many potential sources of environmental contamination, including sex hormones—especially estrogens. The analyzed literature shows that Citation: Wojnarowski, K.; estrone (E1), estradiol (E2), estriol (E3), and synthetic ethinyloestradiol (EE2) are the most significant Podobi´nski,P.; Cholewi´nska,P.; in terms of environmental impact. Potential sources of contamination are, among others, livestock Smoli´nski,J.; Dorobisz, K. Impact of farms, slaughterhouses, and large urban agglomerations. Estrogens occurring in the environment Estrogens Present in Environment on Health and Welfare of Animals. can negatively affect the organisms, such as animals, through phenomena such as feminization, Animals 2021, 11, 2152. https:// dysregulation of natural processes related to reproduction, lowering the physiological condition of doi.org/10.3390/ani11072152 the organisms, disturbances in the regulation of both proapoptotic and anti-apoptotic processes, and even the occurrence of neoplastic processes thus drastically decreasing animal welfare. Unfortunately, Academic Editors: Edward Narayan, the amount of research conducted on the negative consequences of their impact on animal organisms Alan Tilbrook, Dominique Blache, is many times smaller than that of humans, despite the great richness and diversity of the fauna. Shane Maloney and Jill Fernandes Therefore, there is a need for further research to help fill the gaps in our knowledge. Received: 5 June 2021 Keywords: hormones; welfare; animals; estrogens Accepted: 19 July 2021 Published: 20 July 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in published maps and institutional affil- Currently we can observe a growing interest in the state of the environment, methods iations. of its protection, and the impact that the pollutants present in it have on the health of living organisms. Our knowledge of already present and emerging types of pollution is still expanding, but at an insufficient pace. Sex hormones are one of the groups of pollutants that have recently attracted the attention of scientists. The available literature indicates that the most important of them in terms of environmental impact are hormones belonging Copyright: © 2021 by the authors. to the group of estrogens. Estrogens are a group of sex hormones that include estrone Licensee MDPI, Basel, Switzerland. (E1), estradiol (E2), estriol (E3), estetrol (E4)—produced only during pregnancy, and often This article is an open access article distributed under the terms and synthetic ethinyloestradiol (EE2). Estrogens are also called female hormones and they play conditions of the Creative Commons crucial a role in female organisms, but it should be taken into consideration that they are Attribution (CC BY) license (https:// also necessary for proper functioning of male organisms [1]. creativecommons.org/licenses/by/ Estrogens mainly imply their effects by interaction with isoforms of the estrogen 4.0/). receptor (ER)—ERα and ERβ which then bind these hormones in the cytoplasm of cells Animals 2021, 11, 2152. https://doi.org/10.3390/ani11072152 https://www.mdpi.com/journal/animals Animals 2021, 11, 2152 2 of 16 Animals 2021, 11, 2152 2 of 16 Estrogens mainly imply their effects by interaction with isoforms of the estrogen re- ceptor (ER)—ERα and ERβ which then bind these hormones in the cytoplasm of cells and andtransport transport this complex this complex to the to cell the nucleus. cell nucleus. As a result, As a the result, activation the activation of response of response elements elementsin gene promoters in gene promoters begins the begins transcription the transcription process. Aforementioned process. Aforementioned receptors receptorscan be di- canvided be dividedinto nuclear into nuclearestrogen estrogen receptors receptors (nERs) and (nERs) membrane and membrane estrogen estrogen receptors receptors (mERs). (mERs).Beside the Beside “traditional” the “traditional” estrogen estrogen action, addi action,tional additional ways have ways been have described—influence been described— influencethrough cell through signal cell transduction signal transduction tied with mE tiedRs with rather mERs than rathergenomic than activity genomic process. activity The process.available The literature available discusses literature the discusses differences the differences in the affinity in the and affinity mechanism and mechanism of action ofof actionthese receptors, of these receptors, however, however, as shown as by shown the latest by the studies, latest studies,there is therea high is degree a high of degree func- oftional functional and structural and structural similarity similarity between between mERs mERsand nERs and [2]. nERs Recently, [2]. Recently, additional additional recep- receptors,tors, namely, namely, ER-X ER-X and and Erx Erx were were described described in in the the literature literature but but additional researchresearchon on themthem and and mechanisms mechanisms involved involved with with their their action action are are highly highly advised. advised. ThereThere are are many many potential potential sources sources of contaminationof contamination of the of environmentthe environment with with estrogens, estro- suchgens, as such animal as animal farms, farms, slaughterhouses, slaughterhouses, or large or urbanlarge urban agglomerations agglomerations (Figure (Figure1)[ 3,4 ].1) Estrogens[3,4]. Estrogens present present in excreta, in excreta, due to due natural to natural or artificial or artificial processes processes (like hormone (like hormone therapy ther- or contraception)apy or contraception) contaminate, contaminate, by wastewater by wastewater or fertilization, or fertilization, water and water soil. and An soil. additional An ad- factorsditional determining factors determining the degree the of riskdegree resulting of risk from resulting the presence from the of sexpresence hormones of sex in hor- the environmentmones in the are environment their half-life, are which their varies half-lif dependinge, which onvaries the physico-chemical depending on the conditions, physico- thechemical microbiological conditions, richness the microbiological of contaminated ric watershness of and contaminated soil, from 12 waters h to even and 180 soil, days from in the12 caseh to ofeven water 180 reservoirs days in the without case aof stabilized water reservoirs population without of microorganisms a stabilized population [5]. Removal of ofmicroorganisms estrogen from the[5]. aquatic Removal environment of estrogen is fr important,om the aquatic however, environment it is difficult is toimportant, achieve evenhowever, with it the is usedifficult of modern to achieve filtration even with methods the use [6– of8]. modern As evidenced filtration by methods recent research, [6–8]. As microbialevidenced degradation by recent research, of estrogens microbial can bedegrad led byation many of estrogens bacteria strains can be i.e.,led byRhodococcus, many bac- Novosphingobiumteria strains i.e.,, AcinetobacterRhodococcus,, AgromycesNovosphingobium, and Sphingomonas, Acinetobacter, thus, Agromyces showing, possibleand Sphingo- safe andmonas inexpensive, thus showing ways possible for the reduction safe and ofinexpensive threat involved ways withfor the such reduction pollution of [threat9–13]. in- It isvolved worth with noting such that pollution some fungi, [9–13]. mainly It is worth species noting belonging that some to Aspergillus fungi, mainlygenus species are also be- reportedlonging to performAspergillus aerobic genus degradation are also reported of estrogens to perform [9]. Another aerobic threatdegradation related of to estrogens the pres- ence[9]. Another of hormones threat in therelated aquatic to the environment presence of may hormones be the processes in the aq ofuatic their environment accumulation may in bottombe the processes sediments, of from their which accumulation they can bein releasedbottom sediments, again under from appropriate which they physical can be and re- chemicalleased again conditions under [appropriate9–11]. Another physical factor and of riskchemical can be conditions their bioaccumulation [9–11]. Another in living factor organismsof risk can [ 9be,11 their,14,15 bioaccumulation]. in living organisms [9,11,14,15]. FigureFigure 1. 1.Sources Sources of of estrogens estrogens