Investigation of endocrine disruptor pollutants and their metabolites along the Romanian Black Sea Coast: Occurrence, distribution and risk assessment

Highlights

• Organic UV-Filters and Bisphenol derivatives are emerging contaminants in coastal areas of the Romanian Black Sea.

• Both endocrine disruptor classes were found in all three analyzed matrices.

• The distribution patterns of UVFs and BPs in seawater, sediment and algae were investigated.

• Aquatic environmental exposure to UVFs and BPs and their health risks were assessed.

Abstract

In recent years, the occurrence of organic UV-filters (UVFs) and bisphenol derivatives (BPs) in the marine environment has raised high concerns all over the world, due to the potentially adverse impacts on marine organism and, indirectly on human health. This paper reports, for the first time in Romania, the occurrence, distribution pattern and environmental risk assessment of UVFs, BPs and their metabolites in seawater, sediment and algae collected from the Romania Black Sea coastal region. BP-3 (2-hydroxy-4-methoxy-benzophenone) was the most abundant contaminant in seawater samples, with detection frequency of 100 %. Sediment samples were dominated by ES (Ethylhexyl salicylate), with concentration values up to 5823 ng/g d.w., while for algae, concentrations of several hundreds of ng/g d.w. were determined for BP-3, BS (Benzyl salicylate) and BPE (Bisphenol E). Environmental risk assessment revealed that some UVFs and BPs detected in seawater samples were hazardous to the marine organism of the Black Sea.

Introduction

The production and intensive use of synthetic chemicals is a potential threat to environmental health, especially for aquatic ecosystems (Wong et al., 2017; Backhaus et al., 2019; Posthuma et al., 2020). After being used for various purposes, most of these chemicals reach coastal areas. Although, in these areas, anthropogenic contamination poses a significant threat, the determination and characterization of chemical contaminants in coastal areas is limited to a small number of compounds (Basilio et al., 2020; Bayen et al., 2019). Regarding the anthropogenic impacts, the pollution of the marine environment by a huge number of contaminants from urban, industrial and agricultural activities has become an issue of growing concern (Pintado-Herrera and Lara Martín, 2020). Hazardous chemicals, such as organic UV filters (UVFs) and bisphenol analogs (BPs), are new classes of emerging pollutants that have raised significant concerns over the past decade due to their potential threat to the marine environment and human health (Akhbarizadeh et al., 2020; Safakhah et al., 2020; Astel et al., 2020; Cadena-Aizaga et al., 2020). UV filters and bisphenol-type derivatives are two classes of emerging contaminants used in large quantities in a variety of consumer products, including various packaging, pharmaceuticals and personal care products, while both classes of compounds are present simultaneously in plastic products (Asimakopoulos et al., 2016; Karthikraj and Kannan, 2018; Lu et al., 2018). Because of the endocrine disrupting properties associated with various diseases such as obesity, diabetes, thyroid and reproductive system diseases, UVFs and BPs have attracted increased attention from the scientific community following biomonitoring studies published on aquatic and marine ecosystems and even on humans (Asimakopoulos et al., 2014; Yu and Wu, 2014; Rocha et al., 2018).

Organic UV filters represent a wide range of chemicals widely used in various personal care products (PPCPs), such as sunscreens and cosmetics to provide protection against UV radiation. These chemicals are also used in industrial products (insecticides, paints, packaging materials, textiles) that are exposed to sunlight in order to protect them from damage caused by UV light, including discoloration and cracking (Tsui et al., 2017; Xue et al., 2017; Mao et al., 2019). Due to their widespread use in various products, organic UV filters enter aquatic ecosystems both directly (washed from the skin during recreational activities in the environment) and indirectly (wastewater discharges). Their widespread use has led to their ubiquitous presence in lakes, rivers (Corada-Fernández et al., 2017; You et al., 2015), wastewater (Ramos et al., 2016; Ekpeghere et al., 2016; Chiriac et al., 2021b), sludge (Zhang et al., 2011; Gago-Ferrero et al., 2011; Chiriac et al., 2021b), seawater (Tsui et al., 2014; Rodríguez et al., 2015; Mitchelmore et al., 2019; Cadena-Aizaga et al., 2020; Labille et al., 2020; Pintado-Herrera and Lara Martín, 2020) and beach sediments (Huang et al., 2016; Mitchelmore et al., 2019; Astel et al., 2020; Cadena-Aizaga et al., 2020). The risk associated with the presence of these compounds in aquatic ecosystems is mainly due to their negative effects on human health, being recognized for their ability to interfere with the proper functioning of the endocrine system. For example, the most popular organic UV filter, 2-hydroxy-4-methoxy-benzophenone (BP-3), has been shown to have a slight estrogenicity in various in vivo and in vitro studies (Wang et al., 2016; Rodríguez et al., 2015). Moreover, this compound has been shown to have a high degree of toxicity to coral reefs (He et al., 2019). The concern raised by the presence of this compound in the aquatic environment increases with the possibility of their transformation into metabolic by-products, which are often much more dangerous compared to the parent compounds. As example, some of BP-3 (bio)degradation product, 2,4-dihydroxybenzophenone (BP-1), 2,2’,4,4’-tetrahydroxybenzophenone (BP-2), 4-hydroxybenzophenone (4-HBP) and 2,3,4-trihydroxybenzophenone (234-HBP) have a stronger estrogenic activity than the parent compound (Kim and Choi, 2014; Watanabe et al., 2015). These benzophenone derivatives are not only recognized as (bio) degradation products of BP-3, but they are also used as active substances in various products. Moreover, high estrogenic activity has been observed in mammals and fish, for another well-known class of organic UV filters, that of salicylate derivatives (Jimenez-Diaz et al., 2013). Given these considerations, the UVFs worldwide distribution and potential threat to marine organisms have been extensively discussed in a recent review article (Cadena-Aizaga et al., 2020). Therefore, more and more researchers are focusing on the dangers that UVFs pose to marine ecosystems.

Bisphenol analogs are a group of chemicals used as antioxidants and stabilizers in the production of plastics, food packaging and receipts (Molina-Molina et al., 2019; Zhao et al., 2019; Gingrich et al., 2019). BPA is the most known bisphenol analogs widely found in marine environments, due to its widespread use in a variety of products such as adhesives, food and beverage packages, baby feeding bottles, electronic components, plastics, toys, paper coating, flame retardants and building materials (Yang et al., 2019; Akhbarizadeh et al., 2020; Liu et al., 2021). Known for its endocrine disrupting properties, its harmful effects on human health have led to the need to ban or limit this compound (ECHA, 2017; EU, 2016; USEPA, 2014) and replace it with structural analogs with similar physicochemical properties. Among them, Bisphenol S (BPS) is mainly used as a component of phenolic resins and in the production of thermal paper, while, bisphenol B (BPB), bisphenol E (BPE) and bisphenol F (BPF) are used in the production of polycarbonate resins and plastics (Chen et al., 2016; Usman and Ahmad, 2016). Although BPs have been used for their fewer toxic properties than BPA, studies have shown that they can cause side effects similar to those induced by BPA (Chen et al., 2016; Tisler et al., 2016). According to recent studies, bisphenol analogs have negative effects on human health and aquatic and terrestrial organisms similar to BPA in terms of persistence, endocrine disruption, bioaccumulation potential or aquatic toxicity (Chen et al., 2016; Wang et al., 2017).

In recent years, researchers from all over the world have reported the presence of BPs in various environmental components such as wastewater (Sun et al., 2017; Xue and Kannan, 2019; Cesen et al., 2018), sludge (Song et al., 2014; Yu et al., 2015), surface water (Esteban et al., 2014; Wee et al., 2019), seawater (Zhao et al., 2019), sediment (Safakhah et al., 2020) and biota (Barboza et al., 2020; Seoane et al., 2020). The presence of BPs in marine environments increases alarmingly with the spread of marine pollution by plastics, as BPs are constituent chemicals in plastics that are gradually released from plastic into seawater (Safakhah et al., 2020; M’Rabet et al., 2019). However, the main source by which these compounds reach the sea remains via rivers, wastewater treatment plant effluents and leaching from BPs based materials (Im and Loffler, 2016). The Black Sea coast acts as a reservoir for many contaminants from various sources. Seawater and sediments represent the final deposit of organic compounds such as UVFs and BPs. The content and spread of these compounds along the coast can be a danger especially for marine ecosystems but also for human health.

In order to better understand the impact of organic UV filters and bisphenol derivatives on marine environment, this study aimed to: (i) determine the presence of ten UVFs and six BPs in seawater, sediment and algae samples collected from the coastal area of Black Sea from the Romanian territory; (ii) determine the distribution pattern of these endocrine disruptors (EDCs) in the analyzed samples; (iii) environmental risk assessment using concentration values (MEC) measured in this study and toxicity results reported in the literature. This article presents the first study that investigated the contamination degree of different marine environmental compartments (seawater, sediment and algae) along the Black Sea coast with endocrine disruptor chemicals such as UVFs and BPs.