Abstract
The presence of pharmaceuticals in the aquatic environment is a contemporary reality and it is necessary to understand more about the effects of this presence on organisms. The purpose of this work was to assess the ecotoxicity of antibiotics metronidazole, nitrofurantoin, trimethoprim, and sulphamethoxazole (single and mixture) in Vibrio fischeri and Desmodesmus subspicatus at μg L−1 concentrations. The evaluation of the toxic effect of the antibiotics on V. fischeri and D. subspicatus was based on fluorescence and bioluminescence tests, respectively, using nominal concentrations. When tested individually, the four antibiotics gave rise to a toxic effect on the evaluated organisms. Sulphamethoxazole caused a higher toxic effect on V. fischeri and D. subspicatus from 7.81 to 500 μg L−1. Trimethoprim and sulphamethoxazole showed hormesis for the concentrations, which ranged from 7.81 to 62.5 μg L−1. The mixture of antibiotics induced a toxic effect on the V. fischeri and D. subspicatus organisms (from 0.03 to 1 μg L−1 concentrations) than when the antibiotics were evaluated individually. These results were significant since water quality problems are widespread all over the word, and emerging pollutants such as antibiotics have been detected in the aquatic environment in very low concentrations.
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Introduction
Several classes of pharmaceuticals have been identified and quantified in rivers and sewage treatment stations, including antibiotics (Castiglioni et al. 2004; Lin et al. 2008; Leung et al. 2012; Locatelli et al. 2011), analgesics and anti-inflammatory drugs (Bendz et al. 2005; Stackelberg et al. 2007; Gibbons et al. 2011), antihistamines (Stackelberg et al. 2007), stimulants (Lin et al. 2008; Locatelli et al. 2011), lipid regulators (Andreozzi et al. 2005; Lin et al. 2008), anti-hypertension drugs (Stackelberg et al. 2007), beta-blockers (Bendz et al. 2005; Lin et al. 2008; Andreozzi et al. 2005), and antipsychotic drugs (Bendz et al. 2005; Stackelberg et al. 2007; Lin et al. 2008; Loganathan et al. 2009).
The low levels of pharmaceuticals that have been found, varying from ng L−1 to μg L−1, may interfere with biological systems. Some reported effects are: inducing genotoxic effects (Sponchiado et al. 2010; Ragugnetti et al. 2011) and endocrine disruption (Kim et al. 2012) in fish; effects on Daphnia magna population growth rate (Kim et al. 2012; Kim and Lee 2012; Liguoro et al. 2009; Garric et al. 2007; Flaherty and Dodson 2005); reduction in Moina macrocopa adult survival (Kim et al. 2012). Among these compounds, antibiotics attract added interest for their ability to induce bacterial resistance. Several strains of microorganisms that have been isolated from rivers and treatment stations have shown to be resistant to various antibiotics (Silva et al. 2010; Aleem et al. 2003; Dang et al. 2012; Koczura et al. 2012; Luczkiewicz et al. 2010; Costa et al. 2006; Threedeach et al. 2012; Middleton and Salierno 2013). Concern about the effect that antibiotics can cause to the environment goes beyond the induction of multi-resistance. Changes have also been observed in the ovaries of Danio rerio (Madureira et al. 2011) and in the liver of female and male Danio rerio when they were exposed to a mixture of non-steroidal drugs, including sulfamethoxazole (SMX), and trimethoprim (TMP) (Madureira et al. 2012). Among the organisms used to determine the potential ecotoxicological effects of pharmaceuticals in the environment are Daphnia magna, Vibrio fischeri, and Desmodesmus subspicatus (Ioele et al. 2016; You et al. 2016; Dang et al. 2012; Kim et al. 2012; Kim and Lee 2012; Liguoro et al. 2012; Gómez-Ramos et al. 2011). Despite of several organizations charged with biomonitoring and establishing aquatic chemical criteria incorporate these organisms into standard testing protocol guidelines, taking into account concentrations in mg L−1 (OECD 2008, OECD 2011; ABNT 2011, 2012), further studies are lacking to environmental concentrations (ng L−1 and μg L−1) effects on these organisms. Effects like hormesis, which occurs at low concentrations, are not predicted by these methodologies. Zou et al. (2013) observed the effect of hormesis on V. fischeri in a mixture of antibiotics at low concentrations. Liguoro et al. (2010) observed that green algae had higher sensitivity to sulfonamides than did blue algae, which was predicted by the Committee for Medicinal Products for Veterinary Use (CVMP/VICH/790/03 2003).
V. fischeri has been used to evaluate the toxicity of pharmaceuticals. Trovó et al. (2011) used V. fischeri to evaluate the reduction in toxicity of amoxicillin after it was exposed to a photo-Fenton treatment. Similarly, Li et al. (2008) evaluated the reduction in toxicity of tetracycline after treatment with ozonation. Zou et al. (2013) studied the effect of hormesis for mixtures of antibiotics using V. fischeri.
Following this line of investigation, green microalgae have been similarly used (Liguoro et al. 2012; Lanzky and Halling-Sorensen 1997; Liguoro et al. 2010). Liguoro et al. (2012) reported that TMP may induce the CYP1A protein in various tissues of Pseudokirchneriella subcapitata (currently named Raphidocelis subcapitata). Lanzky and Halling-Sorensen (1997) observed acute toxicity of metronidazole (MET) on Chlorella spp. and Selenastrum capricornutum (currently named Raphidocelis subcapitata). Liguoro et al. (2010) showed that sulfaquinoxaline and sulfaguanidine are more toxic to green algae (Pseudokirchneriella subcapitata, Scenedesmus dimophus and Synecocossus leopoliensis).
SMX is an antimicrobial from the sulphonamide class; it competes with ρ-aminobenzoic acid, which is a precursor in the synthesis of folic acid, a key compound for the synthesis of DNA and RNA in bacteria. Sulpha drugs compete for the dihydropteroate synthetase enzyme to inhibit the synthesis of folate. TMP acts on the enzyme dihydrofolate reductase by deceiving it, since its structure is similar to part of folate’s, a substance with which the enzyme interacts. This prevents the formation of tetrahydrofolic acid, which is a substance essential for bacterial and vegetable synthesis. Both drugs are administered together because TMP enhances the effect of SMX (Rang et al. 2011).
The compounds nitrofuranics, MET, and nitrofurantoin (NIT) activate as the nitro-group is reduced, and this leads to the formation of electrophilic species that can react with DNA. The result of this process is the breaking and destabilization of the DNA helix, which can be accelerated when adenine and thymine are present (Bosquesi et al. 2008).
In this study the antibiotics MET, NIT, TMP, and sulphamethoxazole (single and mixture) were tested for their adverse effects on V. fischeri and D. subspicatus to illustrate possible toxic or hormetic effects of pharmaceuticals in the aquatic environment.
Materials and Methods
The evaluation of the toxic effect of antibiotics on the bioindicators V. fischeri and D. subspicatus was based on the methods ISO 11348-1:2007 and ISO 8692 (2012). The toxicity tests were conducted at the Ecotoxicology Laboratory, SENAI-CIC (Serviço Nacional de Aprendizagem Industrial—Cidade Industrial de Curitiba) in Curitiba, Paraná, Brazil.
Standards and Solutions
The following antibiotics were used for the ecotoxicological tests: MET Sigma; NIT, Sigma; SMX Fluka and TMP Sigma-Aldrich. The antibiotic stock solutions (single and mixture) were prepared as following: 1 mg of each antibiotic (single and mixture) were dissolved in 10 mL systems of specific solvents according to the criteria of solubility (NIT in acetone; TMP in chloroform/ methanol, 1:1, v/v; SMX in methanol; and MET in ethanol/methanol 1:1, v/v). Finally the antibiotic stock solutions were completed with milliQ water until 1 L, resulting in an 1 mg L−1 solution.
The antibiotic concentrations were equal or even higher than other authors (Supplementary Material S1) previously reported in rivers for compounds such as SMX (Gros et al. 2012; Vazquez-Roig et al. 2012; Na et al. 2013; Du et al. 2015), TMP (Locatelli et al. 2011; Gros et al. 2012; Vazquez-Roig et al. 2012; Na et al. 2013; Du et al. 2015) and hospital effluents (Santos et al. 2013). Therefore, the effects of these chemicals in aquatic organisms must be analyzed, mainly concerning their significant potential for bioaccumulation (Caminada et al. 2006).
Acute Toxicity Testing
Vibrio fischeri
The test solutions of the single antibiotics were prepared in concentrations ranging from 3.91 to 500 μg L−1 (nominal concentrations) for all the antibiotics in 2% aqueous sodium chloride solution. The concentration of the mixture ranged from 0.03 to 1 μg L−1 (nominal concentrations) for each antibiotic.
The V. fischeri bacterium was grown in a solid culture medium for Photobacterium in the dark, at 22 °C, for a period of 72 h. Prior to use, the culture was observed in the dark to confirm the presence of luminescence. Bioluminescence was measured in a luminometer Lumistox 300 Dr. Langue, using the Lumissoft software. The luminescence inhibition percentage was calculated until 1%. Below 1% the results were considered as negative. The toxicity of the sample was corrected with the correction factor obtained from the non-toxic reference sample (2% NaCl solution).
The exposure time was 30 min (ISO 11348-1:2007) for the solutions containing the antibiotics (single and mixture). One solvent control and three treatments (replicates) were carried out for each concentration. The solvent control contained the same amount of solvent used to prepare the tested concentrations.
Desmodesmus subspicatus
D. subspicatus was chosen since it is a typical organism studied to analyze effects of substances on aquatic organisms, and other authors have observed the effects of antibiotics on this organism as well as on other species of algae.
For this test, the concentrations of aqueous single antibiotic solutions ranged from 7.81 to 1000 μg L−1 (nominal concentrations) and the concentration of the mixtures ranged from 0.03 to 1 μg L−1 (nominal concentrations) for each antibiotic.
The algae were incubated at 23 ± 2 °C under continuous fluorescent light (1120 μEs−1 m−2) and were maintained in suspension by continuous stirring. One control and three treatments (replicates) were carried out for each concentration. The solvent control contained the same amount of solvent used to prepare the tested concentrations.
The results were quantified based on the measurements of chlorophyll by in vivo fluorimetry in a Turner Designs Trilogy fluorometer. The results of chlorophyll a measured in relative fluorescence units were converted to % inhibition using Eq. 1:
where μc is the solvent control luminescence, μe the luminescence of solution with antibiotic.
Statistical Analysis
Statistical analysis was performed using the XLSTAT-2013, an add-on statistical package of Excel. The results were tested using the Shapiro–Wilk, Anderson–Darling, Lilliefors and Jarque-Bera tests. Since the data was not normally distributed, the non-parametric Wilcoxon test was used for the analysis of the results between two populations. For the comparisons between all the antibiotics in all concentrations for the same organism and the solvent control, the non-parametric Kruskal–Wallis test was performed. Differences were considered significant at p < 0.05.
Results and Discussion
Isolated Antibiotics
Vibrio fischeri
An inhibitory effect on V. fischeri by the four tested antibiotics was observed (Fig. 1). The effects of the inhibition of bioluminescence increased with an increase in concentration, p < 0.0001. There was no effect of the solvent controls into the measured bioluminescence.
At 3.91 μg L−1 concentration, TMP had the lowest % inhibition (0.96%), followed by MET (3.21%), NIT (4.70%) and SMX (13.65%). NIT has not been reported in aquatic environments, however various species of bacteria that are resistant to this antibiotic, have been isolated from natural waters and effluents from sewage treatment plants (Aleem et al. 2003; Costa et al. 2006; Luczkiewicz et al. 2010; Dang et al. 2012; Koczura et al. 2012; Threedeach et al. 2012; Middleton and Salierno 2013).
The inhibition values were obtained using an exposure time of 30 min. Although the toxic effects for TMP and MET were much lower than observed for SMX and NIT (4.25 and 3.21 times respectively, Fig. 1), their influence on V. fischeri in field settings cannot be disregarded as it may involve longer contact times. 30 min has been used by other authors to test the effect of other antibiotics on V. fischeri in higher concentrations (Trovó et al. 2011; Li et al. 2008). Otherwise Froehner et al. (2000) noted that for other antibiotics (chloramphenicol, nalidixic acid, and streptomycin sulfate) an inhibition increasing when the test was carried out for 7 and 24 h. According to Froehner et al. (2000), two of those antibiotics had no effect in 30 min.
The concentrations that gave rise to active responses were higher than those measured in effluent from sewage treatment plants and river water: 1.09 μg L−1 of SMX in wastewater (Yang et al. 2005); 0.34 μg L−1 of TMP in effluent (Watkinson et al. 2007); and 0.314 μg L−1 of MET in river water (Leung et al. 2012). Still, further studies with longer testing times should be carried out to compare chronic effects.
There was an increase in inhibition with increased concentrations of the tested antibiotics for NIT and MET. Variations were observed for TMP (concentrations from 0.9 to 500 μg L−1) and SMX (concentrations from 3.91 to 62.5 μg L−1) (Fig. 1a and c). This variation was similar to that reported by Zou et al. (2013), which showed hormetic effects in a range from 253.28 to 25,000 μg L−1 for SMX (p = 0.01) and 29.03 to 2903.20 μg L−1 for TMP. Herein, an instance of hormesis was measured in lower concentrations. The toxicity effect was most evident for TMP, for 0.9 and 1.8 μg L−1 concentrations, with a negative effect from 3.9 to 125 μg L−1 and an increase in the effect from 250 to 500 μg L−1 (p = 0.002). Those toxic effects observed for SMX and TMP suggest the limitation of using only linear models, which determine the lowest observed effect concentrations (LOEC) and the no observable effect concentration (NOEC) to evaluate impacts of pollutants in aquatic environments. For example, Ioele et al. (2016) calculated LOEC for SMX as 95.05–97.03 μg mL−1 (95,050–97,030 μg L−1) and NOEC as 93.01 μg mL−1 (93,010 μg L−1), which do not represent the toxic behavior for this substance, according to the herein studies.
It is important to stress that the concentrations at which effects were observed for TMP and SMX in the present study were below the Predicted no-effect concentration (PNEC) values reported by Kümmerer and Henninger (2003), which were 1.0 and 20 μg L−1, respectively. For MET, the concentrations which resulted in effects were higher than the PNEC values described by Lin et al. (2008) (1.3 μg L−1). However, it should be emphasized that these molecules do not typically occur in an isolated manner in the aquatic environment and the effects of possible mixtures deserves attention.
Desmodesmus subspicatus
The percentage of inhibition of photosynthetic activity of D. subspicatus increased with greater concentrations of the four tested antibiotics (Fig. 2). NIT gave rise to the highest change in inhibition (4.82–89.28%) and SMX to the lowest (73.90–100%).
The concentrations of 250–1000 μg L−1 were considered to be high when compared to concentrations found in the surface water: 1.83 μg L−1 MET; 0.95 μg L−1 SMX; and 0.69 μg L−1 TMP (Valcárcel et al. 2011). For the % of inhibition observed for the lowest concentration, 7.81 μg L−1, NIT gave rise to the lowest inhibition of photosynthetic activity (4.82%), followed by TMP (38.21%), MET (46%) and SMX (73.90%), which was a different result from that which was observed for the higher concentrations. Making such assessments requires considerations of these compounds’ characteristics and their mechanisms of action. Even substances with similar structures and action mechanisms may present different results. Liguoro et al. (2010) evaluated the effect of two sulfonamides for veterinary use (sulphaquinoxaline and sulphaguanidine) in three types of algae and they found different percentage of inhibition for each compound, demonstrating the need to evaluate substances individually, even if they have similar actions.
Although the environmental concentrations of MET, TMP, and SMX described by Valcárcel et al. (2011) were lower than the inhibition concentrations here registered, further studies are needed to understand the chronic effects of the environmental concentrations.
The species of algae used to perform the test should also be considered. The same substance can show different results for different algae. Liguoro et al. (2010) observed that green algae had a higher sensitivity than the blue algae recommended by CVMP/VICH/790/03. In another study, the same authors achieved 20% growth inhibition of P. subcapitata for 6.25 mg L−1 of TMP. In the present study, 38.21% inhibition was observed for the same pharmaceutical, but for another species and at a lower concentration (7.81 μg L−1). Consequently, comparisons of results between different species should be made with caution.
D. subspicatus showed higher sensitivity to MET, with 46% inhibition for the 7.81 μg L−1 concentration, compared to the test performed by Lanzky and Halling-Sorensen (1997) for Selenastrum capricornutun, which found 10% inhibition at a concentration between 19.9 and 21.7 mg L−1. SMX induced a higher percentage of inhibition (Fig. 2), demonstrating the algaecide action of sulfonamides (Liguoro et al. 2010). The SMX algaecide action was higher than the NTR and MET nitro-group (Supplementary Material S2) effect, which could indicate that inhibition mechanism of folate prevails over the destabilization of DNA provoked through the reduction of the nitro-group (Bosquesi et al. 2008).
The changes in the percentage inhibition for the concentrations from 7.81 to 125 μg L−1 obtained for V. fischeri were also observed for D. subspicatus (Fig. 3), with significantly differences: p values equal to 0.04 (MET), 0.03 (TMP) and 0.04 (SMX). Such variations may suggest a similarity to the effect of hormesis (Calebrese and Baldwin 2002; Zou et al. 2013). The variation observed for NIT was not significantly different, p = 0.16.
Mixture of Antibiotics
The mixtures of antibiotics (0.03 to 1 μg L−1) gave rise to higher toxic effects on D. subspicatus (average fluorescence inhibition: 76%) than single antibiotic solutions (at concentrations ranging from 7.81 to 1000 μg L−1). When the antibiotics were tested individually, SMX had the highest effect, with 73.90% inhibition at a concentration of 7.8 μg L−1. According to Liguoro et al. (2010), some sulfonamides may have an algaecide effect at concentrations in the order of μg L−1, and this effect is more prevalent when they are in mixtures (Fig. 4).
The mixture also had an effect on V. fischeri but the variation occurred in a linear form, R 2 = 0.98, with an increase in the concentration. For concentrations below 0.125 μg L−1 no effect was observed, which is the lowest concentration at which an effect of the mixture on V. fischeri was observed. Considering that antibiotics are substances that are intended to interfere with microbial metabolisms, it is to be expected that bacterial communities will be the first aquatic organisms to suffer in the presence of these substances. The results observed in this study were the opposite because V. fischeri suffered less effect than D. subspicatus. This reinforces the algaecide effect of sulfonamides (Liguoro et al. 2010) and the influences of MET and NTR nitro-group (Bosquesi et al. 2008). It was not possible to identify if there was a differentiated effect from the antibiotics, when mixed, on the V. fischeri. The study herein indicated that antibiotic mixtures can elicit effects not observed by single exposures. Flaherty and Dodson (2005) reported the same effect on Daphnia magna for mixtures containing SMX, TMP and other antibiotics. The observed effects for the mixtures are of concern because, in nature, these substances are mixed with others, increasing the possibility of synergistic effects.
Conclusion
The single tested antibiotics affected V. fischeri and D. subspicatus at low concentrations (3.91–500 and 7.81–1000 μg L−1, respectively). SMX had the greatest effect on D. subspicatus, while NIT had on V. fischeri. At low concentrations (0.03–1 μg L−1), the mixture caused a greater effect on D. subspicatus, than on V. fischeri compared to observations for the single antibiotics.
The results obtained allow for the identification of the aquatic toxicity of NIT, MET, SMX and TMP at concentration levels from μg L−1 to ng L−1. It provides useful insights to the pharmaceutical industry for refining the ecological information on the safety data sheet for these compounds. NIT ecotoxicological data are not available, and for MET, SMX, and TMP are reported at mg L−1.
References
ABNT (2011) NBR 12648: ecotoxicologia aquática: toxicidade crônica – método de ensaio com algas (Chlorophyceae). Rio de Janeiro, p 28
ABNT (2012) NBR 15411-1: ecotoxicologia aquática – determinação do efeito inibitório de amostras aquosas sobre a emissão de luz de Vibrio scheri (Ensaio de bactéria luminescente) Parte 1: método utilizando bactérias recém-cultivadas. Rio de Janeiro, p 24
Aleem A, Isar J, Malik A (2003) Impact of long-term application of industrial wastewater on the emergence of resistance traits in Azotobacter chroococcum isolated from rhizospheric soil. Bioresour Technol 86:7–13
Andreozzi R, Canterino M, Marotta R, Paxéus NA (2005) Antibiotic removal from wastewaters: the ozonation of amoxicillin. J Hazard Mater 122:243–250
Bendz D, Paxéus NA, Ginn TR, Logec FJ (2005) Occurrence and fate of pharmaceutically active compounds in the environment, a case study: Höje River in Sweden. J Hazard Mater 122:195–204
Bosquesi PL, Almeida AE, Blau L, Menegon RF, Santos JL, Chung MC (2008) Toxicidade de fármacos nitrofurânicos. Rev Ciênc Farm Básica Apl 29(3):231–238
Calebrese E, Baldwin L (2002) Defining hormesis. Hum Exp Toxicol 21:91–97
Caminada D, Escher C, Fent K (2006) Cytotoxicity of pharmaceuticals found in aquatic systems: comparison of PLHC-1 and RTG-2 fish cell lines. Aquat Toxicol 79(2):114–123
Castiglioni S, Fanelli R, Calamari D, Bagnati R, Zuccatoa E (2004) Methodological approaches for studying pharmaceuticals in the environment by comparing predicted and measured concentrations in River Po, Italy. Regul Toxicol Pharm 39:25–32
Costa PM, Vaz-Piresa P, Bernardoc F (2006) Antimicrobial resistance in Enterococcus spp. isolated in inflow, effluent and sludge from municipal sewage water treatment plants. Water Res 40:1735–1740
CVMP/VICH/790/03-FINAL (2003) VICH Topic GL38 (Ecotoxicity Phase II) for Implementation at step 7 Guideline on Environmental impact assessment (EIAS) for veterinary medicinal products—Phase II
Dang Z, Cheng Y, Chen H-M, Cui Y, Yin H-H, Trass T, Montforts M, Vermeire T (2012) Evaluation of the Daphnia magna reproduction test for detecting endocrine disruptors. Chemosphere 88:514–523
Du B, Hadda SP, Scott WC, Chambliss CK, Brooks BW (2015) Pharmaceutical bioaccumulation by periphyton and snails in an effluent-dependent stream during an extreme drought. Chemosphere 119:927–934
Flaherty CM, Dodson S (2005) Effects of pharmaceuticals on Daphnia magna growth and reproduction. Chemosphere 61:200–207
Froehner K, Backhaus T, Grimme LH (2000) Bioassays with Vibrio fischeri for the assessment of delayed toxicity. Chemosphere 40:821–828
Garric J, Vollat B, Duis K, Peålry A, Junker T, Ramil M, Fink G, Ternes TA (2007) Effects of the parasiticide ivermectin on the cladoceran Daphnia magna and the green alga Pseudokirchneriella subcapitata. Chemosphere 69:903–910
Gibbons SE, Wang C, Yinfa MA (2011) Determination of pharmaceutical and personal care products in wastewater by capillary electrophoresis with UV detection. Talanta 84:1163–1168
Gómez-Ramos M, Mezcua M, Agüera A, Fernandez-Alba AR, Gonzalo S, Rodríguez A, Rosal R (2011) Chemical and toxicological evolution of the antibiotic sulfamethoxazole under ozone treatment in water solution. J Hazard Mater 192:18–25
Gros M, Rodríguez-Mozaz S, Barceló D (2012) Fast and comprehensive multi-residue analysis of a broad range of human and veterinary pharmaceuticals and some of their metabolites in surface and treated waters by ultra-high-performance liquid chromatography coupled to quadrupole-linear ion trap tandem mass spectrometry. J Chromatrogr A 1248:104–121
Ioele G, De Luca M, Ragno G (2016) Acute toxicity of antibiotics in surface waters by bioluminescence test. Curr Pharm Anal 12:220–226
ISO 8692 (2012) Water quality-fresh water Algal growth inhibition test with unicellular green algae. International Organization for Standardization, Geneva, p 21
Kim HT, Lee MJ (2012) The individual and population effects of tetracycline on Daphnia magna in multigenerational exposure. Ecotoxicology 21:993–1002
Kim P, Park Y, Ji K, Seo J, Lee S, Choi K, Kho Y, Park J, Choi K (2012) Effect of chronic exposure to acetaminophen and lincomycin on Japanese medaka (Otyzias latipes) and freshwater cladocerans Daphnia magna and Moina macrocopa, and potential mechanisms of endocrine disruption. Chemosphere 89:10–18
Koczura R, Mokracka J, Jabłońska L, Gozdecka E, Kubek M, Kaznowski A (2012) Antimicrobial resistance of integron-harboring Escherichia coli isolates from clinical samples, wastewater treatment plant and river water. Sci Total Environ 414:680–685
Kümmerer K, Henninger A (2003) Promoting resistance by the emission of antibiotics from hospitals and households into influent. Clin Infect Dis 9:1203–1214
Lanzky PF, Halling-Sorensen B (1997) The toxic effect of the antibiotic metronidazole on aquatic organisms. Chemosphere 35:2553–2561
Leung HW, Minh TB, Lam JCW, So MK, Martin M, Lam PKS, Richardson BJ (2012) Distribution, fate and risk assessment of antibiotics in sewage treatment plants in Hong Kong, South China. Environ Int 42:1–9
Li K, Yediler A, Yang M, Schulte-Hostede S, Wong MH (2008) Ozonation of oxytetracycline and toxicological assessment of its oxidation by-products. Chemosphere 72:473–478
Liguoro M, Fioretto B, Poltronieri C, Gallina G (2009) The toxicity of sulfamethazine to Daphnia magna and its additivity to other veterinary sulfonamides and trimethoprim. Chemosphere 75:1519–1524
Liguoro M, Di Leva V, Bona MD, Merlanti R, Caporale G (2012) Sublethal effects of trimethoprim on four freshwater organisms. Ecotoxicol Environ Safe 82:114–121
Liguoro M, Di Leva V, Gallina G, Faccio E, Pinto G (2010) Evaluation of the aquatic toxicity of two veterinary sulfonamides using five test organisms. Chemosphere 81:788–793
Lin AYC, YU T-H, Lin C-F (2008) Pharmaceutical contamination in residential, industrial and agricultural wastewater: risk to aqueous environments in Taiwan. Chemosphere 74:131–141
Locatelli MA, Sodré FF, Jardim WF (2011) Determination of antibiotics in Brazilian surface waters using liquid chromatography-electrospray tandem mass spectrometry. Arch Environ Contam Toxicol 60:385–393
Loganathan B, Phillips M, Mowery H, Jones-Lepp TL (2009) Contamination profiles and mass loadings of macrolide antibiotics and illicit drugs from a small urban wastewater treatment plant. Chemosphere 75:70–77
Luczkiewicz A, Jankowska K, Fudala-Ksiazek S, Olanczuk-Neyman K (2010) Antimicrobial resistance of fecal indicators in municipal wastewater treatment plant. Water Res 44:5089–5097
Madureira TV, Rocha MJ, Cruzeiro C, Galante MH, Monteiro RAF, Rocha E (2011) The toxicity potencial of pharmcaceuticals found in the Douro River estuary (Portugal): assessing impacts on gonadal maturation with a histopathological and stereological study of zebrafish ovary and testis after sub-acute exposures. Aquat Toxicol 105:292–299
Madureira TV, Rocha MJ, Cruzeiro C, Rodrigues I, Monteiro RAF, Rocha E (2012) The toxicity potential of pharmaceuticals found in the Douro River estuary (Portugal): evaluation of imapcts on fish liver, by histopathology, stereology, vitellogenin and CYP1A immunohistochemistry, after sub-acute exposures of the zebrafish model. Environ Toxicol 34:34–45
Middleton J, Salierno JD (2013) Antibiotic resistence in triclosan tolerant fecal coliforms isolated from surface waters near wastewater treatment plant outlows (Morris Country, NJ, USA). Ecotoxicol Environ Safe 88:79–88
Na G, Fang X, Cai Y, Ge L, Zong H, Yuan X, Yao Z, Zhang Z (2013) Occurrence, distribution, and bioaccumulation of antibiotics in coastal environment of Dalian, China. Mar Pollut Bull 69:233–237
OECD (2008) Report of the validation of an enhancement of OECD TG 211: Daphnia magna reproduction test. 93:1–32
OECD (2011) Draft guidance document on standardised test guidelines for evaluating chemicals for endocrine disruption. 1–544
Ragugnetti M, Adams ML, Guimarães ATB, Sponchiado G, de Vasconcelos EC, Oliveira CMR (2011) Ibuprofen Genotoxicity in aquatic environment: an experimental model using Oreochromis niloticus. Water Air Soil Pollut 218:361–364
Rang HP, Dale MM, Ritter JM, Flower RI (2011) Rang & dale farmacologia, 7 ed. Elsevier, Rio de Janeiro
Santos LHMLM, Gros M, Rodriguez-Mozaz S, Delerue-Matos C, Pena A, Barceló D, Montenegro CBSM (2013) Contribution of hospital effluents to the load of pharmaceuticals in urban wastewaters: identification of ecologically relevant pharmaceuticals. Sci Total Environ 461-462:302–3016
Silva TFBX, Ramos DT, Dziedzic M, Oliveira CMR, de Vasconcelos EC (2010) Microbiological quality and antibiotic resistance analysis of a Brazilian water supply source. Water Air Soil Pollut 218:611–618
Sponchiado G, Reynaldo EMFL, Andrade ACB, de Vasconcelos EC, Adam ML, Oliveira CMR (2010) Genotoxic effects in erythrocytes in Oreochromis niloticus exposed to nanograms-per-liter concentration of 17β-estradiol (E2): an assessment using micronucleus and comet assay. Water Air Soil Pollut 218:353–360
Stackelberg PE, Gibs J, Furlong ET, Meyer MT, Zaugg SD, Lippincott RL (2007) Efficiency of convetional drinking-water-treatment process in removal of pharmaceuticals and other organic compounds. Sci Total Environ 377:255–272
Threedeach S, Chiemchaisri W, Watanabe T, Chiemchaisri C, Honda R, Yamamoto K (2012) Antibiotic resistance of Escherichia coli in leachates from municipal solid waste landfills: comparison between semi-aerobic and anaerobic operations. Bioresour Technol 113:253–258
Trovó AG, Nogueira RFP, Agüera A, Fernandez-Alba AR (2011) Degradation of the antibiotic amoxicillin by photo-Fenton process—chemical and toxicological assessment. Water Res 45:1394–1402
Valcárcel Y, Alonso SG, Rodríguez-Gil JL, Gil A, Catalá M (2011) Detection of pharmaceutically active compounds in the rivers and tap water of the Madrid Region (Spain) and potencial ecotoxicological risk. Chemosphere 84:1336–1348
Vazquez-Roig P, Andreu V, Blasco C, Picó Y (2012) Risk assessment on the presence of pharmaceuticals in sediments, soils and waters of the Pego–Oliva Marshlands (Valencia, eastern Spain). Sci Total Environ 440:24–32
Watkinson A, Murby EJ, Costanzo (2007) Removal of antibiotics in conventional and advanced wastewater recycling. Water Res 41:4167–4176
Yang S, Cha J, Carlson K (2005) Simultaneous extraction and analysis of 11 tetracycline and sulfonamide antibiotics in influent and effluent domestic wastewater by solid-phase extraction and liquid chromatography-electrospray ionization tandem mass spectrometry. J Chromatogr A 1097:40–53
You R, Sun H, Yu Y, Lin Z, Qin M, Liu Y (2016) Time-dependent hormesis of chemical mixtures: a case study on sulfa antibiotics and a quorum-sensing inhibitor of Vibrio fischeri. Environ Toxicol Pharmacol 41:45–53
Zou X, Lin Z, Deng Z, Yin D (2013) Novel approach to predicting hormetic effects of antibiotic mixtures on Vibrio fischeri. Chemosphere 90:2070–2076
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We thank the SENAI/PR—Serviço Nacional de Aprendizagem Industrial (Paraná) for their support of this research.
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de Vasconcelos, E.C., Dalke, C.R. & de Oliveira, C.M.R. Influence of Select Antibiotics on Vibrio fischeri and Desmodesmus subspicatus at μg L−1 Concentrations. Environmental Management 60, 157–164 (2017). https://doi.org/10.1007/s00267-017-0841-4
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DOI: https://doi.org/10.1007/s00267-017-0841-4