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H2O2 advanced oxidation
Chemosphere 144 (2016) 989e994
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Biodegradability of iopromide products after UV/H2O2 advanced oxidation Olya S. Keen a, d, *, Nancy G. Love b, Diana S. Aga c, Karl G. Linden a a
Department of Civil, Environmental and Architectural Engineering, University of Colorado, UCB 428, Boulder, CO 80309, USA Civil and Environmental Engineering Department, University of Michigan, Ann Arbor, MI 48109, USA c Chemistry Department, University at Buffalo, The State University of New York, Buffalo, NY 14260, USA d Department of Civil and Environmental Engineering, University of North Carolina, 9201 University City Blvd, Charlotte, NC 28223, USA b
h i g h l i g h t s Iopromide formed biodegradable products after UV/H2O2 treatment. No appreciable mineralization (<1%) occurred during UV/H2O2 treatment. Some of the products were biodegradable to full mineralization. Most of the iopromide transformation in UV/H2O2 is from direct photolysis.
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Article history: Received 3 July 2015 Received in revised form 14 September 2015 Accepted 18 September 2015 Available online xxx
Iopromide is an X-ray and MRI contrast agent that is virtually non-biodegradable and persistent through typical wastewater treatment processes. This study determined whether molecular transformation of iopromide in a UV/H2O2 advanced oxidation process (AOP) can result in biodegradable products. The experiments used iopromide labeled with carbon-14 on the aromatic ring to trace degradation of iopromide through UV/H2O2 advanced oxidation and subsequent biodegradation. The biotransformation assay tracked the formation of radiolabeled 14CO2 which indicated full mineralization of the molecule. The results indicated that AOP formed biodegradable iopromide products. There was no 14C released from the pre-AOP samples, but up to 20% of all radiolabeled carbon transformed into 14CO2 over the course of 42 days of biodegradation after iopromide was exposed to advanced oxidation (compared to 10% transformation in inactivated post-AOP controls). In addition, the quantum yield of photolysis of iopromide was determined using low pressure (LP) and medium pressure (MP) mercury lamps as 0.069 ± 0.005 and 0.080 ± 0.007 respectively. The difference in the quantum yields for the two UV sources was not statistically significant at the 95% confidence interval (p ¼ 0.08), which indicates the equivalency of using LP or MP UV sources for iopromide treatment. The reaction rate between iopromide and hydroxyl radicals was measured to be (2.5 ± 0.2) 109 M1 s1. These results indicate that direct photolysis is a dominant degradation pathway in UV/H2O2 AOP treatment of iopromide. Other iodinated contrast media may also become biodegradable after exposure to UV or UV/H2O2. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Iopromide Advanced oxidation Quantum yield Biodegradation Transformation products
1. Introduction Iopromide is used as an X-ray and MRI contrast medium. It is designed to be biologically inert and is not metabolized as it passes through the body. Ninety percent of administered iopromide is excreted unchanged (Bayer, 2014). Iopromide is resistant to * Corresponding author. Department of Civil and Environmental Engineering, University of North Carolina, 9201 University City Blvd, Charlotte, NC 28223, USA. E-mail address: [email protected] (O.S. Keen). http://dx.doi.org/10.1016/j.chemosphere.2015.09.072 0045-6535/© 2015 Elsevier Ltd. All rights reserved.
conventional wastewater treatment methods due to its biological stability and highly soluble nature. Although iopromide exhibited some biodegradability in bench-scale experiments (Kalsch, 1999, Batt et al., 2006) full-scale studies consistently show that iopromide is one of the few pharmaceuticals completely unaffected by wastewater treatment processes (Ternes and Hirsch, 2000, Carballa et al., 2004). It is also one of the most persistent pharmaceuticals in all of the common drinking water treatment processes (Westerhoff et al., 2005). This remarkable stability makes iopromide one of the most prevalent compounds in wastewater effluents, the
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environment and finished drinking water samples around the world (Ternes and Hirsch, 2000, Kim et al., 2007; Daughton, 2010). Although iopromide is a common and widespread water contaminant, studies have indicated no acute ecotoxic effects to bacteria, algae, crustaceans and fish at concentrations as high as 10 g L1 (Steger-Hartmann et al., 1999). The apparent lack of acute ecotoxicity of the parent compound does not mean that the presence of iopromide in the water cycle has no other undesirable effects. Studies have demonstrated the formation of iodinated disinfection byproducts during chlorination of water containing iodinated contrast media, indicating these are more toxic than currently regulated chlorinated disinfection products (Duirk et al., 2011). Therefore, it is prudent to examine treatment processes capable of removing these compounds from the water cycle. Remarkable stability and persistence in the environment makes iopromide a model compound for studying the effects of chemical treatment processes on biodegradability of persistent chemicals. This study focuses on advanced oxidation process (AOP) in which highly reactive hydroxyl radicals are generated by irradiating water containing hydrogen peroxide (H2O2) with ultraviolet (UV). Prior studies indicate that ozone is not effective for degradation of iopromide (Ternes et al., 2003; Huber et al., 2003). Hydroxyl radicals (HO) are effective for transformation of a broad range of organic molecules. UV/H2O2 AOP can also transform contaminants by direct photolysis from the UV photons emitted in the process. Iopromide in particular has been demonstrated to be susceptible to photolysis with the quantum yield at 254 nm of 0.039 ± 0.004 (Canonica et al., 2008) as well as to reactions with HO with k ¼ (3.3 ± 0.6) 109 M1 s1 at 25 C and k ¼ (3.34 ± 0.14) 109 M1 s1 as reported in 2 separate studies (Huber et al., 2003; Jeong et al., 2010). A full-scale AOP can be effective in reducing the concentrations of trace organic contaminants by orders of magnitude through chemical transformations but without reaching full mineralization. The properties of the transformation products of organic contaminants have long been a concern associated with the full-scale application of AOP. One way to apply AOP for transformation of trace contaminants in a sustainable manner is to couple it with a biological process downstream that could promote full mineralization of the transformation products. Prior studies have demonstrated that advanced oxidation results in biodegradable products of try-alkyl phosphates (Watts and Linden, 2008) and the pharmaceutical carbamazepine (Keen et al., 2012a). The goal of this study was to demonstrate that enhanced biodegradability is a common outcome of molecular transformation during AOP. While the products of iopromide that form during UV photolysis and AOP rez et al., have been extensively investigated (Jeong et al., 2010; Pe 2009; Kwon et al., 2012), their biodegradability as compared to the parent compound have not been assessed. An additional purpose of the study was to measure the quantum yield of photolysis using low pressure and medium pressure mercury vapor lamps. Medium pressure (MP) lamps emit a broad spectrum of UV wavelengths including lower wavelengths of higher energy, commonly capable of causing greater degree of transformation within a molecule. Since iopromide is known to be susceptible to photolysis (Canonica et al., 2008), it is worthwhile to examine its response to a broad spectrum of wavelengths. Wavelengths below 239 nm emitted by MP UV lamps, have not been examined to date. 2. Materials and methods 2.1. Reagents and samples All chemicals used in this experiment were reagent grade.
Sodium azide was manufactured by Alfa Aesar (Ward Hill, MA), and 30% solution of hydrogen peroxide by J.T. Baker, Phillipsburg NJ. A stock solution of 1000 mg L1 (2950 units/mg) of bovine catalase (SigmaeAldrich, St. Louis, MO) was prepared for hydrogen peroxide quenching prior to bioassays. The radiolabeled (hot) iopromide had a specific activity of 0.031 mCi mg1 of iopromide and a total activity of 1.13 mCi in 5 mL of methanol. Radiolabeled iopromide was donated by the Laboratory for Diagnostics, Genetics & Ecotoxicology, Schering AG, Berlin, Germany. The non-radiolabeled (cold) iopromide was from USP (Rockville, MD) Cat. No. 34480. The molecular structure of iopromide and the location of the radiolabeled carbon-14 molecule are pictured in Fig. S1 of Supplemental Information. Wastewater was collected from a local wastewater treatment plant employing nitrifying activated sludge from the secondary clarifier overflow, filtered through 0.2 mm nylon filter (Millipore, Billerica, MA) within an hour of collection time and stored at 4 C until use. The experiment was performed in duplicate in its entirety using effluent from two different collection times to assure that experimental variability was captured. Water quality parameters of the background matrix are listed in Table 1. Activated sludge was collected from the same facility and was stored at 4 C for no longer than 48 h before use. Volatile suspended solids in the activated sludge were measured using Standard Method 2540 and a Pall A/E glass fiber filter (Pall, Port Washington, NY). 2.2. Advanced oxidation and photolysis setup Advanced oxidation and photolysis for the biodegradability study were carried out in a collimated beam apparatus outfitted with 1 kW medium pressure mercury vapor lamp emitting a characteristic UV spectrum in the 200e400 nm range. Incident irradiance was measured at the sample surface using a NIST calibrated radiometer (International Light IL-1700, Peabody, MA). The AOP experiments were carried out in a large crystallization dish capable of holding 1 L volume necessary for the experiment. The dose was calculated using the methodology by Bolton and Linden (2003). The absorbance of the sample was measured with Cary100Bio spectrophotometer (Agilent, Santa Clara, CA). Petri Factor and sample depth were 0.60 and 4.4 cm respectively. Preliminary experiments with cold iopromide and 10 mg L1 H2O2 demonstrated that a fluence of 2400 mJ cm2 was necessary to achieve 90% transformation of the parent compound in the given background matrix. This UV fluence and H2O2 dose were used for the experiments with radiolabeled iopromide which were followed by biodegradability assays. Photolysis experiments for determination of the quantum yield were performed with the medium pressure (MP) lamp (specifications described above) and with a low pressure (LP) mercury vapor collimated beam outfitted with 4 lamps, 15 W each, emitting at around 253.7 nm. The experiments were performed with cold iopromide standard in a 50 mm diameter crystallization dish. Iopromide was dissolved in ultrapure water (arium611-VF, Sartorius Stedim, Bohemia, NY). Sample depth was 1.7 cm, and Petri Table 1 Water quality parameters for effluent used in the study.
Alkalinity, mg L1 as CaCO3 pH, Nitrite, mg L1 as N Nitrate, mg L1 as N Ammonia, mg L1 as N TOC, mg L1 TN, mg L1
WW sample 1
WW sample 2
88 6.3 <0.015 16.2 0.043 17.25 18.15
86 6.6 <0.015 9.88 <0.015 9.50 11.97
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Factors for the MP and LP lamps were 0.97 and 0.93 respectively. Fundamental properties of iopromide relevant to UV/AOP are the compound's reaction rate constant with HO and the quantum yield of photolysis. Reaction rate of iopromide with HO was determined using competition kinetics with para-chlorobenzoic acid (pCBA) as a probe compound. Reaction rate constant of pCBA with HO is well established: kOH,pCBA ¼ 5109 M1 s1 (Buxton et al., 1988). The contribution of direct photolysis to the overall decay of iopromide and pCBA was factored out before the analysis. Average quantum yield of photolysis (QY) in the 200e300 nm range of wavelengths and at 254 nm were calculated using the method described in detail by Sharpless and Linden (2003). More detailed data are available in Supplemental Information. 2.3. Bioassay Bioassay performed in this study has been described in greater detail elsewhere (Keen et al., 2012a). Briefly, samples prior to AOP experiments and samples that underwent AOP treatment as described above were placed in 250 mL amber bottles (200 mL sample volume). Bovine catalase was added at 1 mg L1 concentration and allowed to react with H2O2. The catalase dose and time to quench H2O2 were established in preliminary experiments. The sample bottles were corked with silicone stoppers, each containing two holes for tubing. The inlet tubing delivered 0.2-micron-filtered and humidified air to the sample and the outlet tubing connected the headspace of the sample bottle to two alkaline traps in series (Fig. 1). The alkaline traps were 60 mL amber glass bottles containing 50 mL 1 N of potassium hydroxide. Activated sludge was added to the sample to result in 67 ± 1 mg L1 of VSS. Any CO2 that forms during mineralization of the organic compounds in solution (including 14CO2 from 14Clabeled iopromide) was trapped in the alkaline solution as the air gets pushed from the sample bottle into the bottles with alkaline solution during the sample aeration. Dissolved CO2 that reacts with water to form H2CO3 quickly deprotonates in alkaline solution and gets trapped in non-volatile form. The second trap was added to capture any carryover from the first trap, but the results showed that the first trap was very efficient and virtually no carryover to the next trap was detected. The amount of radioactivity in the sample and the traps was monitored with liquid scintillation counting (described in subsequent sections) over a period of 42 days. Each sample was compared with a corresponding abiotic control, in which bacteria was inactivated with a 0.01 M sodium azide biocide, and a biotic control not containing iopromide, which was also used as a baseline blank. In a previous study on the biodegradability of carbamazepine post-AOP, we found that no bacterial acclimation was necessary at 1 mg L1 concentration of the compound (Keen et al., 2012a). Iopromide is an X-ray contrast agent and is designed not to have an acute biological effect at high concentrations. Therefore, acclimation of activated sludge to iopromide was deemed unnecessary. In fact, iopromide showed no toxic effects at concentrations as high as
Fig. 1. Schematic of the bioassay setup.
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10 g L1, during short-term toxicity tests with bacteria, algae, and crustaceans (Steger-Hartmann et al., 1999). 2.4. Carbon-14 analysis A Packard 1600 TR liquid scintillation counter was used to measure the radioactivity of the samples. Perkin Elmer (Waltham, MA) Ultima Gold scintillation cocktail was selected due to its efficiency with alkaline solutions as reported by the manufacturer. Sample to cocktail ratio selection procedure and the instrument detection limits have been discussed in prior related published work (Keen et al., 2012a). The radioactivity signal was at least 70 times the instrument detection limit. The selected sample to cocktail ratio was 0.1 mL sample to 6.9 mL cocktail for the wastewater samples, and 1 mL sample to 6 mL cocktail for the traps. 2.5. Liquid chromatography and mass spectrometry Agilent 1100 series high performance liquid chromatography (HPLC) instrument coupled with Agilent XCT plus ion trap (Agilent, Santa Clara, CA) was used to measure the change in the concentration of cold iopromide and pCBA to determine the quantum yield, the reaction rate constant between iopromide and HO, and to determine the required UV fluence to achieve 90% transformation of the parent iopromide in the effluent matrix. The HPLC instrument was equipped with an Agilent XDB-C8 column (4.6 50 mm, 1.8 mm particle size), kept at 30 C and a diode array detector set at 234 nm. Iopromide was analyzed with the MS detector, and pCBA was analyzed using the diode array detector. The MS instrument was equipped with an electrospray ion source. Fullscan (m/z 50-1000) in positive ion mode was performed. The eluent consisted of HPLC grade water (Honeywell Burdick & Jackson, Morristown, NJ) with 0.1% formic acid (Fluka, St. Louis, MO) as Solvent A and HPLC grade acetonitrile (Honeywell Burdick & Jackson, Morristown, NJ) as Solvent B. The elution gradient was 10% Solvent B and 90% Solvent A to 100% Solvent B over 13 min followed by 2 min at 100% Solvent B at 0.4 mL/min flow rate. The post-run equilibration time was 5 min. Sample injection volume was 40 mL. 3. Results and discussion The quantum yields were determined to be 0.080 ± 0.007 for the MP lamp and 0.069 ± 0.005 for the LP lamp. The values represent the means of 3 replicates and the 95% confidence intervals. The difference in the quantum yields for the two UV sources was not statistically significant (t-test with the 95% confidence interval, p ¼ 0.08), which indicates the equivalency of using LP or MP UV sources for iopromide treatment. Prior studies reported the quantum yield at 254 nm of 0.039 ± 0.004 and at the 239e334 nm range of 0.030 ± 0.010 (Canonica et al., 2008) which is almost a factor of 2 lower than the values determined in this study. Some of the discrepancy in the quantum yields for medium pressure lamps is likely related to the range of wavelengths that was taken into account in the calculations: this study determined the quantum yield at 200e300 nm. Different UV irradiance measuring methods were used in the two studies may have led to potential differences in calculated values. The study by Canonica et al. (2008) used atrazine actinometry, while this study used a NIST-calibrated radiometer. Fig. S2 of Supplemental Information shows the molar absorption coefficients for iopromide. It has an absorbance peak at 242 nm with the coefficient of 29,000 M1 cm1. Molar absorption coefficient at 254 nm is 21,000 M1 cm1. The reaction rate constant between iopromide and hydroxyl radicals was established to be (2.5 ± 0.2) 109 M1 s1 in this study. Previous studies report a value of (3.3 ± 0.6) 109 M1 s1 at
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25 C. The difference in values is not significant within the margin of error in both studies. Fig. 2 shows the results of direct photolysis using an MP lamp and AOP using an MP lamp and 10 mg L1 of H2O2 in ultrapure water (A) and in effluent (B). It is evident from the results that in general direct photolysis is very effective for degradation of iopromide. And both direct photolysis and AOP can achieve considerable decrease in iopromide concentrations at UV fluence used in full scale AOP systems with fluence in the 1500e2000 mJ cm2 range. In the experiments with wastewater, the difference between AOP and photolysis was even lower due to HO generated from nitrate photolysis under MP lamp (Keen et al., 2012b). Based on the results, approximately 15% of iopromide can be transformed at a virus inactivation disinfection dose of 186 mJ cm2 in the wastewater matrix after secondary treatment. When radioactivity of the solution was measured, it was revealed that very little, if any, mineralization was achieved during transformation of iopromide. The test was performed in triplicate in effluent at the 2400 mJ cm2 UV fluence and 10 mg L1 H2O2 dose demonstrated to transform 90% of iopromide (cold iopromide results are shown in Fig. 2). The results showed that 98.6 ± 0.5% of radioactivity remained in the liquid sample at 95% confidence interval, and about 1% was mineralized based on the measured 14CO2 release. The results in Fig. S3 of Supplemental Information show the radioactivity signal in the liquid sample before and after hot iopromide solution has been subjected to AOP. In bioassay, the iopromide parent compound showed no mineralization after 42 days of biodegradation, as expected. The sample treated with AOP, on the other hand, showed up to 20% mineralization during the same period with about half of it attributable to non-biological pathways as seen in the control (Fig. 3). At least 95% of the radioactivity was accounted for by the liquid sample and the gas trap. No radioactivity was lost from pre-AOP samples spiked with cell culture, so it is unlikely that the unaccounted radioactivity resulted from adsorption to cells. The samples with biodegradation were the ones with up to 5% of unaccounted radioactivity, which most likely was lost as CO2 escaping through the tubing seals. Some CO2 could also have been lost during sampling, although the head space of the sample was vigorously purged into the alkaline trap for at least a minute before opening the top for sample withdrawal. When the mineralization results are plotted with time on the xaxis, it becomes apparent that the rate of mineralization was much faster during the first week, eventually slowing down to the rate
similar to that observed in the controls (Fig. 4). The decay rate in the abiotic control sample is 0.0017 d1, the same rate (0.0017 d1) is observed in the sample with active microorganisms if sample points for Days 14e42 are considered. Between days 0 and 7, the decay rate is 0.0192 d1 e over an order of magnitude higher than in an abiotic control. This suggests that microorganisms in the sample were active for approximately 7 days, after which their activity slowed down and the decay rate decreased to match the abiotic decay rate in the inactivated control. There could be two explanations for this: (a) the microorganisms exhausted the resources that supported their viability; or (b) only a fraction of the products that formed were degradable by biological processes. On Day 28, nutrient broth (15 mg L1 of beef extract and 25 mg L1 of peptone) was added to both sample and control to test whether the mineralization process was limited by the availability of nutrients for the activated sludge bacteria. No considerable increase in the rate of mineralization was observed. The process was most likely limited by the biodegradability of the transformation products. Although 90% of the parent compound was expected to transform into products, some of them may be more amenable to biodegradation than others. It appears that about 15e20% of the formed products readily mineralize, while the rest mineralize at a slower rate and apparently by abiotic processes. Singh et al. (2015) identified a number of transformation products of advanced oxidation of iopromide and indicated which ones of the products are most biodegradable. Sodium azide has the potential to abiotically degrade organic compounds, so a control study was conducted with post-AOP hot iopromide to evaluate whether NaN3 is responsible for the abiotic degradation seen in inactivated controls. Results shown in Fig. 5 indicate that the majority of the mineralization observed in the controls is not from reactions involving azide, but other reactions, possibly hydrolysis of some of the smaller oxidation products of iopromide. The samples in this control study contained no microorganisms and the water was likely sterile after AOP due to the high dose of UV received. Deiodination of the parent compound has been demonstrated rez et al., 2009) to be the by other studies (Jeong et al., 2010; Pe primary photodegradation and advanced oxidation pathway. Dehalogentation of an organic compound may make it more attractive to microorganisms as substrate. However, recent research shows that even some of the iopromide transformation products that contain 3 iodine atoms can be biodegradable (Singh et al., 2015). Further research is necessary to evaluate the factors that limit full mineralization of the transformation products.
Fig. 2. Decrease in iopromide in ultrapure water (A) and secondary treated effluent (B) during direct photolysis with MP lamp and advanced oxidation with MP lamp and 10 mg L1 H2O2.
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Fig. 3. Iopromide mass balance. Light gray color e fraction of radioactivity due to parent compound and products still in solution. Black color e fraction of radioactivity that migrated into the KOH traps as CO2, i.e. fraction of the radiolabeled compound fully mineralized. The values are the means of the two replicates with error bars representing the standard deviation between the two samples. Left - samples; right - controls (Sample þ NaN3); top e before AOP; bottom e after AOP. The y-axis starts at 0.60 rather than 0 for a clearer view of the extent of biodegradation.
Fig. 4. Decrease in the radioactivity in the post-AOP sample with and without biological activity.
Fig. 5. Abiotic mineralization of AOP transformation products of iopromide with and without NaN3 used for microorganism inactivation in the controls.
4. Conclusions Iopromide is one compound in the class of iodinated contrast media. Other iodinated contrast media compounds could possibly follow a similar transformation pathway via photolysis and AOP
and form biodegradable or hydrolysable products. Future work is needed to determine whether direct photolysis alone can generate biodegradable products or whether presence of hydroxyl radicals is necessary.
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Acknowledgments This research was funded by Water Environment Research Foundation grant U2R11 to the University of Colorado Boulder. Olya Keen was supported in part by EPA STAR graduate fellowship (FP 91713601). The views expressed in this paper are solely those of the authors and have not been reviewed or endorsed by the EPA. The authors would like to thank undergraduate researcher Andrea Berlinghof for her help with the experiments. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.chemosphere.2015.09.072. References Batt, A.L., Kim, S., Aga, D.S., 2006. Enhanced biodegradation of iopromide and trimethoprim in nitrifying activated sludgey. Environ. Sci. Technol. 40 (23), 7367e7373. Bayer, 2014. Ultravist Nonionic Iodinated Radiographic Contrast Medium. Bolton, J.R., Linden, K.G., 2003. Standardization of methods for fluence (UV dose) determination in bench-scale UV experiments. ASCE J. Environ. Eng. 209e215. Buxton, G.V., Greenstock, C.L., Helman, W.P., Ross, A.B., 1988. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (.OH/.O) in aqueous solution. J. Phys. Chem. Reference Data 17, 513e886. Canonica, S., Meunier, L., von Gunten, U., 2008. Phototransformation of selected pharmaceuticals during UV treatment of drinking water. Water Res. 42 (1e2), 121e128. Carballa, M., Omil, F., Lema, J.M., Llompart, M.a., Garcıa-Jares, C., Rodrıguez, I., mez, M., Ternes, T., 2004. Behavior of pharmaceuticals, cosmetics and horGo mones in a sewage treatment plant. Water Res. 38 (12), 2918e2926. Daughton, C.G., 2010. In: Halden, R. (Ed.), Contaminants of Emerging Concern in the Environment: Ecological and Human Health Considerations. American Chemical Society, Washington, DC, pp. 9e68. Duirk, S.E., Lindell, C., Cornelison, C.C., Kormos, J., Ternes, T.A., Attene-Ramos, M., Osiol, J., Wagner, E.D., Plewa, M.J., Richardson, S.D., 2011. Formation of toxic iodinated disinfection by-products from compounds used in medical imaging. Environ. Sci. Technol. 45 (16), 6845e6854. Huber, M.M., Canonica, S., Park, G.-Y., von Gunten, U., 2003. Oxidation of
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pharmaceuticals during ozonation and advanced oxidation processes. Environ. Sci. Technol. 37 (5), 1016e1024. Jeong, J., Jung, J., Cooper, W.J., Song, W., 2010. Degradation mechanisms and kinetic studies for the treatment of X-ray contrast media compounds by advanced oxidation/reduction processes. Water Res. 44 (15), 4391e4398. Kalsch, W., 1999. Biodegradation of the iodinated X-ray contrast media diatrizoate and iopromide. Sci. Total Environ. 225 (1e2), 143e153. Keen, O.S., Baik, S., Linden, K.G., Aga, D.S., Love, N.G., 2012a. Enhanced biodegradation of carbamazepine after UV/H2O2 advanced oxidation. Environ. Sci. Technol. 46 (11), 6222e6227. Keen, O.S., Love, N.G., Linden, K.G., 2012b. The role of effluent nitrate in trace organic chemical oxidation during UV disinfection. Water Res. 46 (16), 5224e5234. Kim, S.D., Cho, J., Kim, I.S., Vanderford, B.J., Snyder, S.A., 2007. Occurrence and removal of pharmaceuticals and endocrine disruptors in South Korean surface, drinking, and waste waters. Water Res. 41 (5), 1013e1021. Kwon, M., Yoon, Y., Cho, E., Jung, Y., Lee, B.-C., Paeng, K.-J., Kang, J.-W., 2012. Removal of iopromide and degradation characteristics in electron beam irradiation process. J. Hazard. Mater. 227e228 (0), 126e134. rez, S., Eichhorn, P., Ceballos, V., Barcelo , D., 2009. Elucidation of photoPe transformation reactions of the X-ray contrast medium iopromide under simulated solar radiation using UPLC-ESI-QqTOF-MS. J. Mass Spectrom. 44 (9), 1308e1317. Sharpless, C.M., Linden, K.G., 2003. Experimental and model comparisons of lowand medium-pressure Hg lamps for the direct and H2O2 assisted UV photodegradation of N-nitrosodimethylamine in simulated drinking water. Environ. Sci. Technol. 37 (9), 1933e1940. Singh, R.R., Lester, Y., Linden, K.G., Love, N.G., Atilla-Gokcumen, G.E., Aga, D.S., 2015. Application of metabolite profiling tools and time-of-flight mass spectrometry in the identification of transformation products of iopromide and iopamidol during advanced oxidation. Environ. Sci. Technol. 49 (5), 2983e2990. €nge, R., Schweinfurth, H., 1999. Environmental risk assessSteger-Hartmann, T., La ment for the widely used iodinated X-Ray contrast agent iopromide (Ultravist). Ecotoxicol. Environ. Saf. 42 (3), 274e281. Ternes, T.A., Hirsch, R., 2000. Occurrence and behavior of X-ray contrast Media in sewage facilities and the aquatic environment. Environ. Sci. Technol. 34 (13), 2741e2748. Ternes, T.A., Stüber, J., Herrmann, N., McDowell, D., Ried, A., Kampmann, M., Teiser, B., 2003. Ozonation: a tool for removal of pharmaceuticals, contrast media and musk fragrances from wastewater? Water Res. 37 (8), 1976e1982. Watts, M., Linden, K., 2008. Photooxidation and subsequent biodegradability of recalcitrant tri-alkyl phosphates TCEP and TBP in water. Water Res. 42 (20), 4949e4954. Westerhoff, P., Yoon, Y., Snyder, S., Wert, E., 2005. Fate of endocrine-disruptor, pharmaceutical, and personal care product chemicals during simulated drinking water treatment processes. Environ. Sci. Technol. 39 (17), 6649e6663.
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Biodegradability of iopromide products after UV/H2O2 advanced oxidation Olya S. Keen a, d, *, Nancy G. Love b, Diana S. Aga c, Karl G. Linden a a
Department of Civil, Environmental and Architectural Engineering, University of Colorado, UCB 428, Boulder, CO 80309, USA Civil and Environmental Engineering Department, University of Michigan, Ann Arbor, MI 48109, USA c Chemistry Department, University at Buffalo, The State University of New York, Buffalo, NY 14260, USA d Department of Civil and Environmental Engineering, University of North Carolina, 9201 University City Blvd, Charlotte, NC 28223, USA b
h i g h l i g h t s Iopromide formed biodegradable products after UV/H2O2 treatment. No appreciable mineralization (<1%) occurred during UV/H2O2 treatment. Some of the products were biodegradable to full mineralization. Most of the iopromide transformation in UV/H2O2 is from direct photolysis.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 July 2015 Received in revised form 14 September 2015 Accepted 18 September 2015 Available online xxx
Iopromide is an X-ray and MRI contrast agent that is virtually non-biodegradable and persistent through typical wastewater treatment processes. This study determined whether molecular transformation of iopromide in a UV/H2O2 advanced oxidation process (AOP) can result in biodegradable products. The experiments used iopromide labeled with carbon-14 on the aromatic ring to trace degradation of iopromide through UV/H2O2 advanced oxidation and subsequent biodegradation. The biotransformation assay tracked the formation of radiolabeled 14CO2 which indicated full mineralization of the molecule. The results indicated that AOP formed biodegradable iopromide products. There was no 14C released from the pre-AOP samples, but up to 20% of all radiolabeled carbon transformed into 14CO2 over the course of 42 days of biodegradation after iopromide was exposed to advanced oxidation (compared to 10% transformation in inactivated post-AOP controls). In addition, the quantum yield of photolysis of iopromide was determined using low pressure (LP) and medium pressure (MP) mercury lamps as 0.069 ± 0.005 and 0.080 ± 0.007 respectively. The difference in the quantum yields for the two UV sources was not statistically significant at the 95% confidence interval (p ¼ 0.08), which indicates the equivalency of using LP or MP UV sources for iopromide treatment. The reaction rate between iopromide and hydroxyl radicals was measured to be (2.5 ± 0.2) 109 M1 s1. These results indicate that direct photolysis is a dominant degradation pathway in UV/H2O2 AOP treatment of iopromide. Other iodinated contrast media may also become biodegradable after exposure to UV or UV/H2O2. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Iopromide Advanced oxidation Quantum yield Biodegradation Transformation products
1. Introduction Iopromide is used as an X-ray and MRI contrast medium. It is designed to be biologically inert and is not metabolized as it passes through the body. Ninety percent of administered iopromide is excreted unchanged (Bayer, 2014). Iopromide is resistant to * Corresponding author. Department of Civil and Environmental Engineering, University of North Carolina, 9201 University City Blvd, Charlotte, NC 28223, USA. E-mail address: [email protected] (O.S. Keen). http://dx.doi.org/10.1016/j.chemosphere.2015.09.072 0045-6535/© 2015 Elsevier Ltd. All rights reserved.
conventional wastewater treatment methods due to its biological stability and highly soluble nature. Although iopromide exhibited some biodegradability in bench-scale experiments (Kalsch, 1999, Batt et al., 2006) full-scale studies consistently show that iopromide is one of the few pharmaceuticals completely unaffected by wastewater treatment processes (Ternes and Hirsch, 2000, Carballa et al., 2004). It is also one of the most persistent pharmaceuticals in all of the common drinking water treatment processes (Westerhoff et al., 2005). This remarkable stability makes iopromide one of the most prevalent compounds in wastewater effluents, the
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environment and finished drinking water samples around the world (Ternes and Hirsch, 2000, Kim et al., 2007; Daughton, 2010). Although iopromide is a common and widespread water contaminant, studies have indicated no acute ecotoxic effects to bacteria, algae, crustaceans and fish at concentrations as high as 10 g L1 (Steger-Hartmann et al., 1999). The apparent lack of acute ecotoxicity of the parent compound does not mean that the presence of iopromide in the water cycle has no other undesirable effects. Studies have demonstrated the formation of iodinated disinfection byproducts during chlorination of water containing iodinated contrast media, indicating these are more toxic than currently regulated chlorinated disinfection products (Duirk et al., 2011). Therefore, it is prudent to examine treatment processes capable of removing these compounds from the water cycle. Remarkable stability and persistence in the environment makes iopromide a model compound for studying the effects of chemical treatment processes on biodegradability of persistent chemicals. This study focuses on advanced oxidation process (AOP) in which highly reactive hydroxyl radicals are generated by irradiating water containing hydrogen peroxide (H2O2) with ultraviolet (UV). Prior studies indicate that ozone is not effective for degradation of iopromide (Ternes et al., 2003; Huber et al., 2003). Hydroxyl radicals (HO) are effective for transformation of a broad range of organic molecules. UV/H2O2 AOP can also transform contaminants by direct photolysis from the UV photons emitted in the process. Iopromide in particular has been demonstrated to be susceptible to photolysis with the quantum yield at 254 nm of 0.039 ± 0.004 (Canonica et al., 2008) as well as to reactions with HO with k ¼ (3.3 ± 0.6) 109 M1 s1 at 25 C and k ¼ (3.34 ± 0.14) 109 M1 s1 as reported in 2 separate studies (Huber et al., 2003; Jeong et al., 2010). A full-scale AOP can be effective in reducing the concentrations of trace organic contaminants by orders of magnitude through chemical transformations but without reaching full mineralization. The properties of the transformation products of organic contaminants have long been a concern associated with the full-scale application of AOP. One way to apply AOP for transformation of trace contaminants in a sustainable manner is to couple it with a biological process downstream that could promote full mineralization of the transformation products. Prior studies have demonstrated that advanced oxidation results in biodegradable products of try-alkyl phosphates (Watts and Linden, 2008) and the pharmaceutical carbamazepine (Keen et al., 2012a). The goal of this study was to demonstrate that enhanced biodegradability is a common outcome of molecular transformation during AOP. While the products of iopromide that form during UV photolysis and AOP rez et al., have been extensively investigated (Jeong et al., 2010; Pe 2009; Kwon et al., 2012), their biodegradability as compared to the parent compound have not been assessed. An additional purpose of the study was to measure the quantum yield of photolysis using low pressure and medium pressure mercury vapor lamps. Medium pressure (MP) lamps emit a broad spectrum of UV wavelengths including lower wavelengths of higher energy, commonly capable of causing greater degree of transformation within a molecule. Since iopromide is known to be susceptible to photolysis (Canonica et al., 2008), it is worthwhile to examine its response to a broad spectrum of wavelengths. Wavelengths below 239 nm emitted by MP UV lamps, have not been examined to date. 2. Materials and methods 2.1. Reagents and samples All chemicals used in this experiment were reagent grade.
Sodium azide was manufactured by Alfa Aesar (Ward Hill, MA), and 30% solution of hydrogen peroxide by J.T. Baker, Phillipsburg NJ. A stock solution of 1000 mg L1 (2950 units/mg) of bovine catalase (SigmaeAldrich, St. Louis, MO) was prepared for hydrogen peroxide quenching prior to bioassays. The radiolabeled (hot) iopromide had a specific activity of 0.031 mCi mg1 of iopromide and a total activity of 1.13 mCi in 5 mL of methanol. Radiolabeled iopromide was donated by the Laboratory for Diagnostics, Genetics & Ecotoxicology, Schering AG, Berlin, Germany. The non-radiolabeled (cold) iopromide was from USP (Rockville, MD) Cat. No. 34480. The molecular structure of iopromide and the location of the radiolabeled carbon-14 molecule are pictured in Fig. S1 of Supplemental Information. Wastewater was collected from a local wastewater treatment plant employing nitrifying activated sludge from the secondary clarifier overflow, filtered through 0.2 mm nylon filter (Millipore, Billerica, MA) within an hour of collection time and stored at 4 C until use. The experiment was performed in duplicate in its entirety using effluent from two different collection times to assure that experimental variability was captured. Water quality parameters of the background matrix are listed in Table 1. Activated sludge was collected from the same facility and was stored at 4 C for no longer than 48 h before use. Volatile suspended solids in the activated sludge were measured using Standard Method 2540 and a Pall A/E glass fiber filter (Pall, Port Washington, NY). 2.2. Advanced oxidation and photolysis setup Advanced oxidation and photolysis for the biodegradability study were carried out in a collimated beam apparatus outfitted with 1 kW medium pressure mercury vapor lamp emitting a characteristic UV spectrum in the 200e400 nm range. Incident irradiance was measured at the sample surface using a NIST calibrated radiometer (International Light IL-1700, Peabody, MA). The AOP experiments were carried out in a large crystallization dish capable of holding 1 L volume necessary for the experiment. The dose was calculated using the methodology by Bolton and Linden (2003). The absorbance of the sample was measured with Cary100Bio spectrophotometer (Agilent, Santa Clara, CA). Petri Factor and sample depth were 0.60 and 4.4 cm respectively. Preliminary experiments with cold iopromide and 10 mg L1 H2O2 demonstrated that a fluence of 2400 mJ cm2 was necessary to achieve 90% transformation of the parent compound in the given background matrix. This UV fluence and H2O2 dose were used for the experiments with radiolabeled iopromide which were followed by biodegradability assays. Photolysis experiments for determination of the quantum yield were performed with the medium pressure (MP) lamp (specifications described above) and with a low pressure (LP) mercury vapor collimated beam outfitted with 4 lamps, 15 W each, emitting at around 253.7 nm. The experiments were performed with cold iopromide standard in a 50 mm diameter crystallization dish. Iopromide was dissolved in ultrapure water (arium611-VF, Sartorius Stedim, Bohemia, NY). Sample depth was 1.7 cm, and Petri Table 1 Water quality parameters for effluent used in the study.
Alkalinity, mg L1 as CaCO3 pH, Nitrite, mg L1 as N Nitrate, mg L1 as N Ammonia, mg L1 as N TOC, mg L1 TN, mg L1
WW sample 1
WW sample 2
88 6.3 <0.015 16.2 0.043 17.25 18.15
86 6.6 <0.015 9.88 <0.015 9.50 11.97
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Factors for the MP and LP lamps were 0.97 and 0.93 respectively. Fundamental properties of iopromide relevant to UV/AOP are the compound's reaction rate constant with HO and the quantum yield of photolysis. Reaction rate of iopromide with HO was determined using competition kinetics with para-chlorobenzoic acid (pCBA) as a probe compound. Reaction rate constant of pCBA with HO is well established: kOH,pCBA ¼ 5109 M1 s1 (Buxton et al., 1988). The contribution of direct photolysis to the overall decay of iopromide and pCBA was factored out before the analysis. Average quantum yield of photolysis (QY) in the 200e300 nm range of wavelengths and at 254 nm were calculated using the method described in detail by Sharpless and Linden (2003). More detailed data are available in Supplemental Information. 2.3. Bioassay Bioassay performed in this study has been described in greater detail elsewhere (Keen et al., 2012a). Briefly, samples prior to AOP experiments and samples that underwent AOP treatment as described above were placed in 250 mL amber bottles (200 mL sample volume). Bovine catalase was added at 1 mg L1 concentration and allowed to react with H2O2. The catalase dose and time to quench H2O2 were established in preliminary experiments. The sample bottles were corked with silicone stoppers, each containing two holes for tubing. The inlet tubing delivered 0.2-micron-filtered and humidified air to the sample and the outlet tubing connected the headspace of the sample bottle to two alkaline traps in series (Fig. 1). The alkaline traps were 60 mL amber glass bottles containing 50 mL 1 N of potassium hydroxide. Activated sludge was added to the sample to result in 67 ± 1 mg L1 of VSS. Any CO2 that forms during mineralization of the organic compounds in solution (including 14CO2 from 14Clabeled iopromide) was trapped in the alkaline solution as the air gets pushed from the sample bottle into the bottles with alkaline solution during the sample aeration. Dissolved CO2 that reacts with water to form H2CO3 quickly deprotonates in alkaline solution and gets trapped in non-volatile form. The second trap was added to capture any carryover from the first trap, but the results showed that the first trap was very efficient and virtually no carryover to the next trap was detected. The amount of radioactivity in the sample and the traps was monitored with liquid scintillation counting (described in subsequent sections) over a period of 42 days. Each sample was compared with a corresponding abiotic control, in which bacteria was inactivated with a 0.01 M sodium azide biocide, and a biotic control not containing iopromide, which was also used as a baseline blank. In a previous study on the biodegradability of carbamazepine post-AOP, we found that no bacterial acclimation was necessary at 1 mg L1 concentration of the compound (Keen et al., 2012a). Iopromide is an X-ray contrast agent and is designed not to have an acute biological effect at high concentrations. Therefore, acclimation of activated sludge to iopromide was deemed unnecessary. In fact, iopromide showed no toxic effects at concentrations as high as
Fig. 1. Schematic of the bioassay setup.
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10 g L1, during short-term toxicity tests with bacteria, algae, and crustaceans (Steger-Hartmann et al., 1999). 2.4. Carbon-14 analysis A Packard 1600 TR liquid scintillation counter was used to measure the radioactivity of the samples. Perkin Elmer (Waltham, MA) Ultima Gold scintillation cocktail was selected due to its efficiency with alkaline solutions as reported by the manufacturer. Sample to cocktail ratio selection procedure and the instrument detection limits have been discussed in prior related published work (Keen et al., 2012a). The radioactivity signal was at least 70 times the instrument detection limit. The selected sample to cocktail ratio was 0.1 mL sample to 6.9 mL cocktail for the wastewater samples, and 1 mL sample to 6 mL cocktail for the traps. 2.5. Liquid chromatography and mass spectrometry Agilent 1100 series high performance liquid chromatography (HPLC) instrument coupled with Agilent XCT plus ion trap (Agilent, Santa Clara, CA) was used to measure the change in the concentration of cold iopromide and pCBA to determine the quantum yield, the reaction rate constant between iopromide and HO, and to determine the required UV fluence to achieve 90% transformation of the parent iopromide in the effluent matrix. The HPLC instrument was equipped with an Agilent XDB-C8 column (4.6 50 mm, 1.8 mm particle size), kept at 30 C and a diode array detector set at 234 nm. Iopromide was analyzed with the MS detector, and pCBA was analyzed using the diode array detector. The MS instrument was equipped with an electrospray ion source. Fullscan (m/z 50-1000) in positive ion mode was performed. The eluent consisted of HPLC grade water (Honeywell Burdick & Jackson, Morristown, NJ) with 0.1% formic acid (Fluka, St. Louis, MO) as Solvent A and HPLC grade acetonitrile (Honeywell Burdick & Jackson, Morristown, NJ) as Solvent B. The elution gradient was 10% Solvent B and 90% Solvent A to 100% Solvent B over 13 min followed by 2 min at 100% Solvent B at 0.4 mL/min flow rate. The post-run equilibration time was 5 min. Sample injection volume was 40 mL. 3. Results and discussion The quantum yields were determined to be 0.080 ± 0.007 for the MP lamp and 0.069 ± 0.005 for the LP lamp. The values represent the means of 3 replicates and the 95% confidence intervals. The difference in the quantum yields for the two UV sources was not statistically significant (t-test with the 95% confidence interval, p ¼ 0.08), which indicates the equivalency of using LP or MP UV sources for iopromide treatment. Prior studies reported the quantum yield at 254 nm of 0.039 ± 0.004 and at the 239e334 nm range of 0.030 ± 0.010 (Canonica et al., 2008) which is almost a factor of 2 lower than the values determined in this study. Some of the discrepancy in the quantum yields for medium pressure lamps is likely related to the range of wavelengths that was taken into account in the calculations: this study determined the quantum yield at 200e300 nm. Different UV irradiance measuring methods were used in the two studies may have led to potential differences in calculated values. The study by Canonica et al. (2008) used atrazine actinometry, while this study used a NIST-calibrated radiometer. Fig. S2 of Supplemental Information shows the molar absorption coefficients for iopromide. It has an absorbance peak at 242 nm with the coefficient of 29,000 M1 cm1. Molar absorption coefficient at 254 nm is 21,000 M1 cm1. The reaction rate constant between iopromide and hydroxyl radicals was established to be (2.5 ± 0.2) 109 M1 s1 in this study. Previous studies report a value of (3.3 ± 0.6) 109 M1 s1 at
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25 C. The difference in values is not significant within the margin of error in both studies. Fig. 2 shows the results of direct photolysis using an MP lamp and AOP using an MP lamp and 10 mg L1 of H2O2 in ultrapure water (A) and in effluent (B). It is evident from the results that in general direct photolysis is very effective for degradation of iopromide. And both direct photolysis and AOP can achieve considerable decrease in iopromide concentrations at UV fluence used in full scale AOP systems with fluence in the 1500e2000 mJ cm2 range. In the experiments with wastewater, the difference between AOP and photolysis was even lower due to HO generated from nitrate photolysis under MP lamp (Keen et al., 2012b). Based on the results, approximately 15% of iopromide can be transformed at a virus inactivation disinfection dose of 186 mJ cm2 in the wastewater matrix after secondary treatment. When radioactivity of the solution was measured, it was revealed that very little, if any, mineralization was achieved during transformation of iopromide. The test was performed in triplicate in effluent at the 2400 mJ cm2 UV fluence and 10 mg L1 H2O2 dose demonstrated to transform 90% of iopromide (cold iopromide results are shown in Fig. 2). The results showed that 98.6 ± 0.5% of radioactivity remained in the liquid sample at 95% confidence interval, and about 1% was mineralized based on the measured 14CO2 release. The results in Fig. S3 of Supplemental Information show the radioactivity signal in the liquid sample before and after hot iopromide solution has been subjected to AOP. In bioassay, the iopromide parent compound showed no mineralization after 42 days of biodegradation, as expected. The sample treated with AOP, on the other hand, showed up to 20% mineralization during the same period with about half of it attributable to non-biological pathways as seen in the control (Fig. 3). At least 95% of the radioactivity was accounted for by the liquid sample and the gas trap. No radioactivity was lost from pre-AOP samples spiked with cell culture, so it is unlikely that the unaccounted radioactivity resulted from adsorption to cells. The samples with biodegradation were the ones with up to 5% of unaccounted radioactivity, which most likely was lost as CO2 escaping through the tubing seals. Some CO2 could also have been lost during sampling, although the head space of the sample was vigorously purged into the alkaline trap for at least a minute before opening the top for sample withdrawal. When the mineralization results are plotted with time on the xaxis, it becomes apparent that the rate of mineralization was much faster during the first week, eventually slowing down to the rate
similar to that observed in the controls (Fig. 4). The decay rate in the abiotic control sample is 0.0017 d1, the same rate (0.0017 d1) is observed in the sample with active microorganisms if sample points for Days 14e42 are considered. Between days 0 and 7, the decay rate is 0.0192 d1 e over an order of magnitude higher than in an abiotic control. This suggests that microorganisms in the sample were active for approximately 7 days, after which their activity slowed down and the decay rate decreased to match the abiotic decay rate in the inactivated control. There could be two explanations for this: (a) the microorganisms exhausted the resources that supported their viability; or (b) only a fraction of the products that formed were degradable by biological processes. On Day 28, nutrient broth (15 mg L1 of beef extract and 25 mg L1 of peptone) was added to both sample and control to test whether the mineralization process was limited by the availability of nutrients for the activated sludge bacteria. No considerable increase in the rate of mineralization was observed. The process was most likely limited by the biodegradability of the transformation products. Although 90% of the parent compound was expected to transform into products, some of them may be more amenable to biodegradation than others. It appears that about 15e20% of the formed products readily mineralize, while the rest mineralize at a slower rate and apparently by abiotic processes. Singh et al. (2015) identified a number of transformation products of advanced oxidation of iopromide and indicated which ones of the products are most biodegradable. Sodium azide has the potential to abiotically degrade organic compounds, so a control study was conducted with post-AOP hot iopromide to evaluate whether NaN3 is responsible for the abiotic degradation seen in inactivated controls. Results shown in Fig. 5 indicate that the majority of the mineralization observed in the controls is not from reactions involving azide, but other reactions, possibly hydrolysis of some of the smaller oxidation products of iopromide. The samples in this control study contained no microorganisms and the water was likely sterile after AOP due to the high dose of UV received. Deiodination of the parent compound has been demonstrated rez et al., 2009) to be the by other studies (Jeong et al., 2010; Pe primary photodegradation and advanced oxidation pathway. Dehalogentation of an organic compound may make it more attractive to microorganisms as substrate. However, recent research shows that even some of the iopromide transformation products that contain 3 iodine atoms can be biodegradable (Singh et al., 2015). Further research is necessary to evaluate the factors that limit full mineralization of the transformation products.
Fig. 2. Decrease in iopromide in ultrapure water (A) and secondary treated effluent (B) during direct photolysis with MP lamp and advanced oxidation with MP lamp and 10 mg L1 H2O2.
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Fig. 3. Iopromide mass balance. Light gray color e fraction of radioactivity due to parent compound and products still in solution. Black color e fraction of radioactivity that migrated into the KOH traps as CO2, i.e. fraction of the radiolabeled compound fully mineralized. The values are the means of the two replicates with error bars representing the standard deviation between the two samples. Left - samples; right - controls (Sample þ NaN3); top e before AOP; bottom e after AOP. The y-axis starts at 0.60 rather than 0 for a clearer view of the extent of biodegradation.
Fig. 4. Decrease in the radioactivity in the post-AOP sample with and without biological activity.
Fig. 5. Abiotic mineralization of AOP transformation products of iopromide with and without NaN3 used for microorganism inactivation in the controls.
4. Conclusions Iopromide is one compound in the class of iodinated contrast media. Other iodinated contrast media compounds could possibly follow a similar transformation pathway via photolysis and AOP
and form biodegradable or hydrolysable products. Future work is needed to determine whether direct photolysis alone can generate biodegradable products or whether presence of hydroxyl radicals is necessary.
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Acknowledgments This research was funded by Water Environment Research Foundation grant U2R11 to the University of Colorado Boulder. Olya Keen was supported in part by EPA STAR graduate fellowship (FP 91713601). The views expressed in this paper are solely those of the authors and have not been reviewed or endorsed by the EPA. The authors would like to thank undergraduate researcher Andrea Berlinghof for her help with the experiments. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.chemosphere.2015.09.072. References Batt, A.L., Kim, S., Aga, D.S., 2006. Enhanced biodegradation of iopromide and trimethoprim in nitrifying activated sludgey. Environ. Sci. Technol. 40 (23), 7367e7373. Bayer, 2014. Ultravist Nonionic Iodinated Radiographic Contrast Medium. Bolton, J.R., Linden, K.G., 2003. Standardization of methods for fluence (UV dose) determination in bench-scale UV experiments. ASCE J. Environ. Eng. 209e215. Buxton, G.V., Greenstock, C.L., Helman, W.P., Ross, A.B., 1988. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (.OH/.O) in aqueous solution. J. Phys. Chem. Reference Data 17, 513e886. Canonica, S., Meunier, L., von Gunten, U., 2008. Phototransformation of selected pharmaceuticals during UV treatment of drinking water. Water Res. 42 (1e2), 121e128. Carballa, M., Omil, F., Lema, J.M., Llompart, M.a., Garcıa-Jares, C., Rodrıguez, I., mez, M., Ternes, T., 2004. Behavior of pharmaceuticals, cosmetics and horGo mones in a sewage treatment plant. Water Res. 38 (12), 2918e2926. Daughton, C.G., 2010. In: Halden, R. (Ed.), Contaminants of Emerging Concern in the Environment: Ecological and Human Health Considerations. American Chemical Society, Washington, DC, pp. 9e68. Duirk, S.E., Lindell, C., Cornelison, C.C., Kormos, J., Ternes, T.A., Attene-Ramos, M., Osiol, J., Wagner, E.D., Plewa, M.J., Richardson, S.D., 2011. Formation of toxic iodinated disinfection by-products from compounds used in medical imaging. Environ. Sci. Technol. 45 (16), 6845e6854. Huber, M.M., Canonica, S., Park, G.-Y., von Gunten, U., 2003. Oxidation of
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pharmaceuticals during ozonation and advanced oxidation processes. Environ. Sci. Technol. 37 (5), 1016e1024. Jeong, J., Jung, J., Cooper, W.J., Song, W., 2010. Degradation mechanisms and kinetic studies for the treatment of X-ray contrast media compounds by advanced oxidation/reduction processes. Water Res. 44 (15), 4391e4398. Kalsch, W., 1999. Biodegradation of the iodinated X-ray contrast media diatrizoate and iopromide. Sci. Total Environ. 225 (1e2), 143e153. Keen, O.S., Baik, S., Linden, K.G., Aga, D.S., Love, N.G., 2012a. Enhanced biodegradation of carbamazepine after UV/H2O2 advanced oxidation. Environ. Sci. Technol. 46 (11), 6222e6227. Keen, O.S., Love, N.G., Linden, K.G., 2012b. The role of effluent nitrate in trace organic chemical oxidation during UV disinfection. Water Res. 46 (16), 5224e5234. Kim, S.D., Cho, J., Kim, I.S., Vanderford, B.J., Snyder, S.A., 2007. Occurrence and removal of pharmaceuticals and endocrine disruptors in South Korean surface, drinking, and waste waters. Water Res. 41 (5), 1013e1021. Kwon, M., Yoon, Y., Cho, E., Jung, Y., Lee, B.-C., Paeng, K.-J., Kang, J.-W., 2012. Removal of iopromide and degradation characteristics in electron beam irradiation process. J. Hazard. Mater. 227e228 (0), 126e134. rez, S., Eichhorn, P., Ceballos, V., Barcelo , D., 2009. Elucidation of photoPe transformation reactions of the X-ray contrast medium iopromide under simulated solar radiation using UPLC-ESI-QqTOF-MS. J. Mass Spectrom. 44 (9), 1308e1317. Sharpless, C.M., Linden, K.G., 2003. Experimental and model comparisons of lowand medium-pressure Hg lamps for the direct and H2O2 assisted UV photodegradation of N-nitrosodimethylamine in simulated drinking water. Environ. Sci. Technol. 37 (9), 1933e1940. Singh, R.R., Lester, Y., Linden, K.G., Love, N.G., Atilla-Gokcumen, G.E., Aga, D.S., 2015. Application of metabolite profiling tools and time-of-flight mass spectrometry in the identification of transformation products of iopromide and iopamidol during advanced oxidation. Environ. Sci. Technol. 49 (5), 2983e2990. €nge, R., Schweinfurth, H., 1999. Environmental risk assessSteger-Hartmann, T., La ment for the widely used iodinated X-Ray contrast agent iopromide (Ultravist). Ecotoxicol. Environ. Saf. 42 (3), 274e281. Ternes, T.A., Hirsch, R., 2000. Occurrence and behavior of X-ray contrast Media in sewage facilities and the aquatic environment. Environ. Sci. Technol. 34 (13), 2741e2748. Ternes, T.A., Stüber, J., Herrmann, N., McDowell, D., Ried, A., Kampmann, M., Teiser, B., 2003. Ozonation: a tool for removal of pharmaceuticals, contrast media and musk fragrances from wastewater? Water Res. 37 (8), 1976e1982. Watts, M., Linden, K., 2008. Photooxidation and subsequent biodegradability of recalcitrant tri-alkyl phosphates TCEP and TBP in water. Water Res. 42 (20), 4949e4954. Westerhoff, P., Yoon, Y., Snyder, S., Wert, E., 2005. Fate of endocrine-disruptor, pharmaceutical, and personal care product chemicals during simulated drinking water treatment processes. Environ. Sci. Technol. 39 (17), 6649e6663.