Review
Mutagens in surface waters: a review

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Abstract

A review of the literature on the mutagenicity/genotoxicity of surface waters is presented in this article. Subheadings of this article include a description of sample concentration methods, mutagenic/genotoxic bioassay data, and suspected or identified mutagens in surface waters published in the literature since 1990. Much of the published surface water mutagenicity/genotoxicity studies employed the Salmonella/mutagenicity test with strains TA98 and/or TA100 with and/or without metabolic activation. Among all data analyzed, the percentage of positive samples toward TA98 was approximately 15%, both in the absence and the presence of S9 mix. Those positive toward TA100 were 7%, both with and without S9 mix. The percentage classified as highly mutagenic (2500–5000 revertants per liter) or extremely mutagenic (more than 5000 revertants per liter) was approximately 3–5% both towards TA98 and TA100, regardless of the absence or the presence of S9 mix. This analysis demonstrates that some rivers in the world, especially in Europe, Asia and South America, are contaminated with potent direct-acting and indirect-acting frameshift-type and base substitution-type mutagens. These rivers are reported to be contaminated by either partially treated or untreated discharges from chemical industries, petrochemical industries, oil refineries, oil spills, rolling steel mills, untreated domestic sludges and pesticides runoff. Aquatic organisms such as teleosts and bivalves have also been used as sentinels to monitor contamination of surface water with genotoxic chemicals. DNA modifications were analyzed for this purpose. Many studies indicate that the 32P-postlabeling assay, the single cell gel electrophoresis (comet) assay and the micronucleus test are sensitive enough to monitor genotoxic responses of indigenous aquatic organisms to environmental pollution. In order to efficiently assess the presence of mutagens in the water, in addition to the chemical analysis, mutagenicity/genotoxicity assays should be included as additional parameters in water quality monitoring programs. This is because according to this review they proved to be sensitive and reliable tools in the detection of mutagenic activity in aquatic environment.

Many attempts to identify the chemicals responsible for the mutagenicity/genotoxicity of surface waters have been reported. Among these reports, researchers identified heavy metals, PAHs, heterocyclic amines, pesticides and so on. By combining the blue cotton hanging method as an adsorbent and the O-acetyltransferase-overproducing strain as a sensitive strain for aminoarenes, Japanese researchers identified two new type of potent frameshift-type mutagens, formed unintentionally, in several surface waters. One group has a 2-phenylbenzotriazole (PBTA) structure, and seven analogues, PBTA-type mutagens, were identified in surface waters collected at sites below textile dyeing factories and municipal wastewater treatment plants treating domestic wastes and effluents. The other one has a polychlorinated biphenyl (PCB) skelton with nitro and amino substitution group and it was revealed to be 4-amino-3,3′-dichloro-5,4′-dinitrobiphenyl derived from chemical plants treating polymers and dye intermediates. However, the identification of major putative mutagenic/genotoxic compounds in most surface waters with high mutagenic/genotoxic activity in the world have not been performed. Further efforts on chemical isolation and identification by bioassay-directed chemical analysis should be performed.

Introduction

Surface waters, such as rivers, lakes and seas, receive large quantities of waste water from industrial, agricultural, and domestic sources, including municipal sewage treatment plants. These surface waters, which contain many unknown compounds, are used as a source of drinking water, as well as for agricultural, recreational and religious activities around the world. Consequently, water pollution can be a serious public health and aquatic ecosystem problem [1], [2], [3], [4], [5], [6]. The US EPA's Toxic Release Inventory (TRI) for 2001 reported that more than 100,000 metric tonnes of chemicals are released into surface waters and approximately 762,000 metric tonnes of chemicals are emitted into the atmosphere annually by industrial use in the United States as shown in Table 1 [7]. This data show that large quantities of toxic materials are routinely released directly or indirectly (via airborne emission) into aquatic systems after industrial usage. Table 1 also notes that more than fifty percent of annual water discharges to aquatic systems come from the chemical, metal smelting and processing, and petroleum refining industries. Moreover, 800 metric tonnes of chemicals released into surface waters and 60,000 metric tonnes of chemicals emitted into the atmosphere are carcinogens ranked as 1, 2A or 2B under the IARC classification system, and most of them are known to have mutagenic and/or clastogenic activity as shown in Table 2 [8], [9], [10]. These carcinogens are categorized into two types: persistent compounds, which include metals and polycyclic aromatic compounds; and volatile compounds. Most chemicals emitted into the atmosphere eventually reach the ground or surface waters through deposition, so these TRI results show that surface waters are readily contaminated with a variety of known mutagenic or genotoxic carcinogens.

Mutagenic/genotoxic compounds, including carcinogens, whether known or unknown, become the components of complex environmental mixtures that can have adverse health effects on humans and indigenous biota [11]. We know quite a lot about identified contaminants, and it is relatively easy to study the sources and fate of those contaminants that have been identified as priorities for concern and control. Post-emission fate and behavior of polycyclic aromatic hydrocarbons (PAHs) in complex mixtures including surface waters have widely investigated throughout the world, because PAHs are identified contaminants and are relatively easy to study the sources and fate [12]. However, few studies have investigated the identification of novel putative mutagens and the quantification of their response concentrations.

On the other hand, the use of short-term bioassays, which can detect a wide range of chemical substances that may produce genetic damage, has permitted the quantification of mutagenic hazard without a priori information about identity or physical–chemical property. In studies of the mutagenicity/genotoxicity of surface water and aquatic biota conducted in the late 1970s, Parry et al. [13] reported on mutagenicity studies on the tissue of the mussel Mytilus edulis in the marine environment, and Pelon et al. [14] reported on the mutagenicity/genotoxicity of Mississippi River water samples by the Salmonella assay developed by Ames et al. [15]. Cytogenic damage in fish exposed to the industrially contaminated Rhine River were also observed [16], [17]. Since 1980, many researchers have assessed mutagenicity/genotoxicity of surface waters using a variety of bioassays and analytical methods from the standpoint of determining the potential contribution to the mutagenic hazards of treated drinking water and potential ecological hazard. Collectively, mutagenicity evaluations of surface water provide an indication of potential hazard in the absence of priority knowledge about the identification or physical/chemical properties of the putative toxicants. The Salmonella mutagenicity assay in particular has been widely used to detect mutagenic activity in complex environmental mixtures such as surface waters, especially river waters.

In the early 1990s, Stahl [18], De Flora et al. [19] and Houk [1] reviewed the genotoxic and/or carcinogenic hazards of natural waters, the marine environment, and industrial wastes and effluents. Houk [1] and Stahl [18] demonstrated that genotoxic organic compounds can enter surface waters from a wide range of industrial and municipal sources by summarizing their genotoxic data performed by short-term genetic bioassays on literature. They also stressed the importance of bioassays to detect mutagenicity/genotoxicity arising from the ubiquity of genotoxic compounds in the environment and the necessity of the identification of the sources of contaminants. White and Rasmussen [4] noted that volumetric emissions from municipal wastewater treatment plants in large urban centers often exceed 109 l per day. As a result, genotoxic loadings from municipal wastewater treatment facilities are often far greater than those of industrial facilities, and there is a strong relationship between a measure of human activity (i.e., population) and surface water genotoxicity. The work of Houk [1] and White et al. [3], [4], [5], [6] implicated a wide range of industries in the release of complex mutagenic mixtures for which the identity of the putative mutagens is not known. On the other hand, some researchers have reported that conventional wastewater purification processes do not effectively remove many chemical contaminants, and treatment may actually increase the mutagenicity/genotoxicity of waste waters [2], [20], [21], [22], [23]. Other studies show a sharp rise in the mutagenicity/genotoxicity of water samples collected at sites downstream from wastewater treatment plants [24], [25]. Consequently, the increasing use of contaminated surface waters and an increase in the magnitude of the contamination pose a serious problem for the health and welfare of humans and indigenous aquatic biota. Thus, appropriate bioassay have been needed for evaluation of surface waters on potential hazard to human and the water environment.

The purpose of this review is to summarize the state of the current literature on mutagenicity/genotoxicity data for surface waters and to lead the most profitable directions for future research in order to control and manage effectively our water environment. In this review, we will focus on a synopsis of the mutagenicity/genotoxicity assay data in surface waters in the scientific literature published since 1990. Subheadings include a description of sample concentration methods, mutagenic/genotoxic bioassay data, and suspected or identified mutagens in surface waters. In most cases, surface waters have been administered in their crude extracts to these biological test system. Fig. 1 illustrates a breakdown of the collected surface water mutagenicity/genotoxicity assays. Results from 178 published mutagenicity/genotoxicity assays of surface waters were obtained from 128 publications. Published mutagenicity/genotoxicity assessments were divided into two major categories: bacterial assays, including the Salmonella mutagenicity test, and the SOS Chromotest and Salmonella umu-test; and aquatic organism and plant assays, including the micronucleus assay, 32P-postlabelling, the comet assay and the alkaline unwinding assay. The 32P-postlabeling assay, DNA strand breaks and the micronucleus test are unique in that they can be utilized in the laboratory setting, or they can be taken to the site for in situ monitoring using fishes or plants that inhabit regions contaminated by industrial and municipal wastewater. Genotoxic parameters (e.g. hepatic DNA adducts) are currently the most valuable biomarkers for environmental risk assessment and there are many reports on the studies linking the DNA damage to subsequent molecular, cellular and tissue-level alteration of aquatic organisms. In this paper, we intended to review the studies in which bioassays with DNA alterations, e.g. mutagenicity, DNA damaging activity and chromosome aberration, as their endpoints were used to evaluate contamination of surface water with genotoxic chemicals. The studies on the tumor incidence or the incidence of idiopathic lesions, including oncogene activation, link to mutagens exposure in aquatic organisms are not cited.

Section snippets

Sample concentration of surface waters for mutagenicity/genotoxicity assays

Mutagenicity/genotoxicity data of surface waters performed using the bacterial assays are summarized in Table 3. There are many varieties of monitoring methods combined with mutagenicity/genotoxicity tests and selective extraction methodologies for identifying the possible classes of mutagenic/genotoxic organic contaminants in surface waters. A discussion of different extraction/concentration methods has been presented in detail by Houk [1] and Stahl [18]. We describe here briefly the sample

Mutagenic features of surface waters with Salmonella typhimurium TA98 and TA100

There are many assays for detecting the mutagenicty/genotoxicity of surface waters, but the utilization of bioassays with bacteria has proven to be very effective for monitoring because these assays are sensitive, inexpensive, reliable, and can be performed in a short period of time with relatively low cost. Among the microbial bioassays, the Salmonella mutagenicity test has been the most widely used for detecting mutagenicity/genotoxicity in surface waters. The different responses of the

Suspected or identified mutagens in surface waters

Numerous chemicals are released directly into surface waters from industrial, domestic and agricultural sources, or following treatment. Surface runoff and atmospheric deposition also contribute to aquatic pollution. These xenobiotic contaminants are generally present in complex mixtures, and many genotoxic chemicals have been detected. Several heavy metals including arsenic, cadmium, chromium, nickel and lead, are known to be genotoxic in vitro [185] and in vivo [186]. Twenty-five surface

Mutagenic/genotoxic bioassay data on surface waters

Thousands of synthetic chemical compounds are currently registered for use in industry, commerce, agriculture and the home, and thousands of tonnes of these are produced annually in the world. Portions of these chemicals are released either deliberately or unintentionally into the atmosphere, land, rivers, lakes and seas, and numerous xenobiotics are ultimately found in the surface waters and sediments. It has been estimated that there are approximately 80,000 chemicals in commerce, and the

Conclusion

Mutagenicity/genotoxicity test of complex mixtures such as surface waters using variety of bioassays demonstrates that these environmental mixtures contain many unidentified and unregulated toxicants which may have carcinogenicity and a risk of unknown magnitude. It can be concluded that the analysis of surface waters proved to be an essential stage of the study to identify areas potentially contaminated by genotoxic compounds from the different sources. In literatures analyzed, some rivers in

Acknowledgements

The authors gratefully acknowledge Paul A. White of Health Canada, Ottawa for inviting this review and Virgina Houk of US EPA in Research Triangle Park, NC for her revision of the English.

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