Occurrence, toxicity and endocrine disrupting potential of Bisphenol-B and Bisphenol-F: A mini-review

Toxicology Letters 312 (2019) 222–227

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Occurrence, toxicity and endocrine disrupting potential of Bisphenol-B and Bisphenol-F: A mini-review Afia Usman, Shoeb Ikhlas, Masood Ahmad

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Department of Biochemistry, Faculty of Life Sciences, Aligarh Muslim University, Aligarh, 202002, India

A R T I C LE I N FO

A B S T R A C T

Keywords: Bisphenol-F Bisphenol-B Endocrine disruption Bisphenol-A analogues

Recent imposition of restriction on the use of Bisphenol-A (BPA) paved the way for entry of its analogues in the market. Bisphenol-B and Bisphenol-F are the major analogues of commercial value. Thus, their increasing production and application make them vulnerable to human exposure. Since these analogues have been recently reported to show toxic properties similar to BPA, so they have attracted remarkable scientific attention. This mini-review summarizes the recent reports on the occurrence, toxicity and endocrine disruption of these two BPA analogues.

1. Introduction

2. Bisphenol-B

Bisphenol-A, a common plasticizer and high production chemical, due to its extensive environmental and human exposure, endocrine disruption and toxicity brought the attention of various government organizations. A 2008 report of National Toxicology Program (NTP) expressed “some concern for effects on the brain, behavior, and prostate gland in fetuses, infants, and children at current human exposures to bisphenol A” (Shelby, 2008). With the help of ToxCast program EPA put BPA at the third highest Toxicological Priority Index (ToxPi) among the 309 environmental chemicals (Reif et al., 2010). The U.S Food and Drug Administration (FDA) shared the opinions of NTP in 2010 (FDA, 2010). This led to the imposition of ban on the use of BPA in baby bottles by various government organizations (EFSA, 2015; FDA, 2013, 2012; Government of Canada, 2010; Michałowicz, 2014). Ever since the implementation of new legislation regarding the BPA use, BPA has been replaced with its analogues such as Bisphenol-F and Bisphenol-B. The production of these analogues is increasing and will continue to do so in near future. Since the analogues are structurally similar to BPA it is expected that they may have same toxicological and endocrine disruptive effects on biological systems. Therefore, there is an important question whether this shift from BPA to its analogues is safe or not. This mini-review summarizes the studies on the occurrence, toxicity and endocrine disruption studies of Bisphenol-F and Bisphenol-B. Table 1 provides the molecular structure and details of BPA, BPB and BPF.

Bisphenol-B (2,2-bis(4-hydroxyphenyl)butane) is another bisphenol-A congener and is used for manufacturing epoxy resins (Cunha and Fernandes, 2010). Structurally it has an ethyl group on the central carbon atom instead of a methyl group found in BPA. In comparison to BPA it was found to show slow aerobic and anaerobic biodegradation (Chang et al., 2014; Ike et al., 2006). It is potential migrant and food contaminant. The presence of BPB in various products such as canned food (Alabi et al., 2014), beverages (Cunha et al., 2011), seafood (Cunha et al., 2012), peeled tomatoes (Grumetto et al., 2008), powdered infant formula (Cunha et al., 2011) and commercial milk (Grumetto et al., 2013), indicates its dietary exposure in humans. BPB has been found to undergo oxidative metabolism in the presence of S9 fraction (Okuda et al., 2011; Yoshihara et al., 2004). In the human urine BPB was detected only after deconjugation using β-glucuronidase enzyme suggesting that the metabolism of BPB occurred mainly through conjugation with glucronic acid or sulfate (Cunha and Fernandes, 2010) (Fig. 1).

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2.1. Environmental contamination and human exposure BPB has been detected in various environmental samples such as wastewaters in China and Croatia (Česen et al., 2019; Zheng et al., 2015), sediment samples (Liao et al., 2012b; Song et al., 2017) and indoor dust (Liao et al., 2012a). It has also been found in human urine, saliva and sera indicating daily burden and internal exposure (Cobellis et al., 2009; Cunha and Fernandes, 2010; Russo et al., 2018a; Song

Corresponding author. E-mail address: masoodamua@rediffmail.com (M. Ahmad).

https://doi.org/10.1016/j.toxlet.2019.05.018 Received 6 March 2019; Received in revised form 16 May 2019; Accepted 21 May 2019 Available online 25 May 2019 0378-4274/ © 2019 Elsevier B.V. All rights reserved.

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Fig. 1. The molecular structure and details of bisphenols.

dental sealants, industrial floors, grouts, electrical varnishes, coatings, lacquers, plastics and adhesives (Rochester and Bolden, 2015). BPF has been detected in several consumer products, especially a major contaminant in personal care products (Liao and Kannan, 2014b; Lu et al., 2018). It has also been detected in beverages and energy drinks (Cacho et al., 2012; Gallart-Ayala et al., 2011; Mandrah et al., 2017; Regueiro and Wenzl, 2015a; Yang et al., 2014b), canned food (Cao and Popovic, 2015; Yang et al., 2014b), ready-made meals (Regueiro and Wenzl, 2015b), food contact recycle paper (Pérez-Palacios et al., 2012), household waste paper and paper products (Jurek and Leitner, 2017; Pivnenko et al., 2015), commercial milk (Grumetto et al., 2013) and pantyhose (Li and Kannan, 2018). BPF has also been recorded as a predominant bisphenol contaminant in foodstuffs (meat and meat products, fish and seafood, vegetables etc.) accounting for 17% of the total bisphenols (Liao and Kannan, 2014a, 2013). Like BPA, BPF is absorbed by oral route and distributed to the whole organism including the reproductive tracts and the fetuses by crossing the placental barrier. A metabolic profiling study on BPF found it to be mainly excreted through the urine but 7–9% of the dose was found to be present in the tissues 96 h after the administration of single oral dose to rats. Also the main metabolite found in the urine was its sulfate conjugate (Cabaton et al., 2006). Similarly, in vitro biotransformation with human and rat liver subcellular fractions led to the formation of BPFglucuronide and BPF-sulfate. Moreover, in vitro metabolism into sulfate and glucuronide conjugate also occurs in HepG2 cell lines (hepatoma cell lines), LS174 T cell lines (intestinal cell lines) and human hepatocytes (Audebert et al., 2011; Dumont et al., 2011). However, hydroxylation was the major metabolic pathway with the occurrence of di-, ortho, and meta-hydroxylated BPF metabolites. BPF-dimers formation has also been documented (Cabaton et al., 2008). Just like their parent compound BPA, both bisphenols (BPB and BPF) undergo detoxification in vivo via conjugation with glucuronic acid and sulfate so as to be made more hydorphilic in order to be excreted out.

et al., 2017). The sera of 27.6% Italian endometric women with a concentration range of 0.88–11.94 × 103 μg/l suggested a relationship between endometriosis and BPB exposure (Cobellis et al., 2009). Estimated daily dietary intake came out to be 2.05 ng/kg bw/day for male and 2.06 ng/kg bw/day for female in Chinese adults (Liao and Kannan, 2014a). 2.2. Toxicity and endocrine disruption studies so far BPB possesses more acute toxicity than BPA (Chen et al., 2002). Moreover, it is slightly more cytotoxic than BPA (Russo et al., 2018b). BPB can induce gene activation of p53 suggesting that it possesses genotoxic potential also (Rosenmai et al., 2014). BPB has been demonstrated to be estrogenic and anti-androgenic chemical (Kitamura et al., 2005; Usman and Ahmad, 2016). It also promoted cell growth presumably by inducing estrogen response element (ERE)-mediated transcription (Mesnage et al., 2017). BPB was also found to exert higher estrogenic activity than BPA via non-genomic G-protein coupled estrogen receptor (GPER) pathway at nanomolar concentrations (Cao et al., 2017). Owing to its estrogenic behaviour, BPB also exhibited zebrafish developmental toxicity (Catron et al., 2018). It was noted that more hydrophobic nature of BPB than BPA actually increased its estrogen activity (Hashimoto et al., 2001; Kitamura et al., 2005). In terms of estrogenicity BPB was found to be metabolically activated (Hashimoto et al., 2001; Okuda et al., 2011; Yoshihara et al., 2001). It was as anti-androgenic as BPA in NCl-H295R cell lines and also significantly decreased testosterone production in adult human testis explants in culture (Desdoits-Lethimonier et al., 2017; Rosenmai et al., 2014). Exposure of BPB in adult rats was reported to cause oxidative stress in testis. It also caused decrease in sperm motility, daily sperm production and number of sperms in epididymis leading to disturbance in the reproductive function (Ullah et al., 2018b, 2018a). BPB is a stronger agonist of human Pregnane-Xreceptor than BPA (Sui et al., 2012). It also causes decrease in cortisol and corticosterone levels (Rosenmai et al., 2014).

3.1. Environmental exposure

3. Bisphenol-F

Due to its chemical similarity with BPA (e.g. log Kow: 3.06; water solubility 360 mg/l), BPF was expected to follow the same environmental distribution as that of BPA (Fromme et al., 2002). Hence, BPF has been found in various environmental matrices, such as sewage sludge (Fromme et al., 2002; Song et al., 2014; Yu et al., 2015), river water (Stachel et al., 2003; Yang et al., 2014), sediments (Liao et al., 2012b; Stachel et al., 2003; Wang et al., 2017; Yang et al., 2014), indoor dust (Xue et al., 2016), waste water treatment plant influents and effluents (Česen et al., 2018; Lee et al., 2015; Sun et al., 2018; Xue and Kannan, 2019), drinking water (Rajasärkkä et al., 2016), surface and ground water (Fromme et al., 2002; Herrero-Hernández et al., 2013), lake (Jin and Zhu, 2016), soil, lettuce (Margenat et al., 2018), dump

Bisphenol-F or BPF with a chemical name of bis(4-hydroxyphenyl) methane also belongs to the bisphenol family. Structurally it possesses two phenol rings which are linked through methylene. BPF is being increasingly used due to low viscosity and better resistance to solvents than BPA epoxy resins (Lu et al., 2018). Consequently, its production is increasing in many countries (Lee et al., 2015). BPF has found a wide range of applications in the industrial sector with its use in manufacturing epoxy resins and polycarbonates; and has been gradually replacing BPA (Liao and Kannan, 2014a; Molina-Molina et al., 2013). It has, therefore, found its application in food packaging, pipe linings, 223

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effects and induced aromatase enzyme activity in zebrafish embryo and vitellogenin synthesis in zebrafish adults (Le Fol et al., 2017; Mu et al., 2018), and disrupted the vertebrate development in Xenopus laevis (Zhu et al., 2018). BPF exposure in the early life stages of zebrafish (Danio rerio) caused adverse effects to the sexual differentiation (Yang et al., 2018a, 2018b). It also impaired reproductive function in zebrafish by causing reduction in number of eggs as well as hatching, and survival rate enhanced E2 production in males and females (Yang et al., 2017). BPF was also found to affect the 5α-reductase (5α-R), a key enzyme involved in neurosteroidogenesis and genes related to dopamine (DA) and serotonin (5-HT) system in the prefrontal cortex of juvenile female rats, and increase in anxiety and depressive behavior in mice offspring due to maternal exposure (Castro et al., 2015; Ohtani et al., 2017).

runoff, compost water and manure (Fromme et al., 2002). 3.2. Human exposure Although the exposure of BPF is mainly anthropogenic in nature but it has been identified as a natural product in mustard (Zoller et al., 2016). Its environmental contamination can lead to its transport into biological systems. Recently, Andra et al. (2015) reviewed the presence of various BPA analogues in human matrices. BPF was found in the human plasma at concentrations three times higher than BPA which suggested a shift in its use vis-à-vis BPA (Kolatorova Sosvorova et al., 2017). It has been detected in urine in several studies (Andrianou et al., 2016; Asimakopoulos et al., 2016; Rocha et al., 2018; Yang et al., 2014a; Ye et al., 2015; Zhang et al., 2016; Zhou et al., 2014). National Health and Nutrition Examination Survey (NHANES) 2013–2014 reported BPF in 66.5% of the urine samples in adults and children (Lehmler et al., 2018). It has also been detected in urine samples from first time mothers (Gyllenhammar et al., 2017), pregnant women (Heffernan et al., 2016; Machtinger et al., 2018), first and second trimester pregnant women and three months postpartum women (Liu et al., 2018; Philips et al., 2018). Its intake via inhalation was found to be 9.48 ng/day (Xue et al., 2016). It has also been detected in breast milk, maternal and cord plasma (Kolatorova et al., 2018; Niu et al., 2017). BPF has also been detected in the human hypothalamus and white matter suggesting that it can cross the blood brain barrier (Charisiadis et al., 2018). Its estimated daily dietary intake in Chinese adults was calculated to be 96.5 ng/kg bw/day in males and 102 ng/kg bw/day in females (Liao and Kannan, 2014a).

3.3.4. Oxidative toxicity BPF has been reported to be moderately toxic in vitro in various cell lines such as adenocarcinoma cells (MCF-7), human cervical epithelial cancer cells (HeLa), mouse fibroblasts (3T3-L1) and rat glioma cells (C6) (Audebert et al., 2011; Russo et al., 2018b). An in vivo study reported its ability of causing liver toxicity (Higashihara et al., 2007). Under in vitro conditions, it promoted cell proliferation via induction of ERα and also elevated reactive oxygen species (ROS) as well as Ca2+ levels (Lei et al., 2018b, 2018a). Especially in human erythrocytes in vitro, BPF induced haemolysis, methaemoglobin formation and stomatocytosis; it also increased cytosolic Ca2+ levels, internal viscosity, osmotic fragility, ROS formation, acetylcholine esterase (AChE), calpain and caspase-3 activities. Above all, it also caused a decrease in the ATP levels and Na+/K+ ATPase activity in human RBCs (Maćczak et al., 2017b, 2017a, 2016, 2015). Another set of studies conducted on Peripheral Blood Mononuclear Cells (PBMCs) in vitro reported that BPF caused a decrease in ATP levels, cell viability and transmembrane mitochondrial potential; caused alterations in size and granulation; enhanced ROS formation, increased cytosolic Ca2+ levels, caspases 8, 9, 3 activites and PARP-1 [poly(ADP-ribose)polymerase-1] and thereby induced apoptosis (Michałowicz et al., 2015; Mokra et al., 2015). Moreover, in vivo studies also found BPF to induce ROS generation in marine rotifer, Branchionus koreanus, juvenile common carp (Carpinus carpio), zebrafish and rats testes (Park et al., 2018; Qiu et al., 2018a, 2018b; Ullah et al., 2018b).

3.3. Toxicity studies on BPF so far conducted 3.3.1. Mutagenicity and genotoxicity BPF was found to be non-mutagenic in salmonella tester strains (Fic et al., 2013). However, it has been recently suggested to be potentially carcinogenic via other tests (F. Yang et al., 2018a, 2018b). Moreover, BPF was reported to have genotoxic potential in HepG2 cell lines (Audebert et al., 2011), chicken DT40 cell lines (Lee et al., 2013) and MCF-7 cell lines (Lei et al., 2018b). In peripheral blood mononuclear cells (PBMCs), it induced SSB (single strand breaks) (Mokra et al., 2017) and oxidative lesions in DNA bases (Mokra et al., 2018).

4. Conclusion 3.3.2. Endocrine disruption A review on BPF’s endocrine disrupting potential revealed it to be as hormonally active as BPA (Rochester and Bolden, 2015). Various studies have demonstrated it to act as estrogenic (Goldinger et al., 2015; Lei et al., 2018a; Mesnage et al., 2017), progesteronic (Feng et al., 2016) and anti-androgenic (Roelofs et al., 2015) in nature. There are conflicting reports on its binding ability to glucocorticoid receptor (GR); while one study suggested that it acts as an agonist (Kolšek et al., 2015), another found it to be antagonistic to GR (Roelofs et al., 2015). Even, it binds to peroxisome proliferator activated receptor α (PPAR α) (Zhang et al., 2017). Moreover, it also causes thyroid endocrine disruption by binding to thyroid receptor (TRβ) (Zhang et al., 2018); increasing the levels of thyroid stimulating hormones (TSH) and altering the T3 and T4 levels (Huang et al., 2016). BPF, just like BPA, was able to influence hormonal regulation (Verbanck et al., 2017). In a human breast cancer cell line it has been demonstrated that BPF poses the risk of cancer progression as much as BPA (Kim et al., 2017).

The ban on BPA led to its replacement by its analogues such as Bisphenol-F and Bisphenol-B. The production and application of these analogues are expected to increase in future. We have, therefore, taken an overview of the reports of last decade on BPB and BPF which suggest the enhanced human exposure and environmental contamination of these analogues. Recent reports have clearly emphasized these analogues to possess endocrine disrupting potential and to cause oxidative and developmental toxicities. The studies conducted so far suggest that these analogues act in a way parallel to their parent compound and are not sound replacements. Conflict of interest The authors declare no conflict of interest. Transparency document The Transparency document associated with this article can be found in the online version.

3.3.3. Developmental toxicity In zebrafish larvae BPF has been found to induce a variety of morphological defects such as cardiac edema, craniofacial abnormality, spinal malformation, cranial hemorrhage, yolk sac deformity and decline in pigmentation; it has also disrupted glucose metabolism by impairing insulin signaling transduction which leads to hyperglycemia (Moreman et al., 2017; Zhao et al., 2018). It showed developmental

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