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Occurrence and Source Apportionment of Sulfonamides and Their Metabolites in Liaodong Bay and the Adjacent Liao River Basin, North China

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Environmental Toxicology and Chemistry, Vol. 30, No. 6, pp. 1252–1260, 2011 # 2011 SETAC Printed in the USA DOI: 10.1002/etc.508 OCCURRENCE AND SOURCE APPORTIONMENT OF SULFONAMIDES AND THEIR METABOLITES IN LIAODONG BAY AND THE ADJACENT LIAO RIVER BASIN, NORTH CHINA AI JIA,JIANYING HU,* XIAOQIN WU,HUI PENG,SHIMIN WU, and ZHAOMIN DONG Laboratory for Earth Surface Processes, College of Urban and Environmental Sciences, Peking University, Beijing, China (Submitted 8 August 2010; Returned for Revision 10 October 2010; Accepted 6 January 2011) Abstract—The presence of antibiotics in the environment is of great concern because of their potential for resistance selection among pathogens. In the present study we investigated the occurrence of 19 sulfonamides, five N-acetylated sulfonamide metabolites, and trimethoprim in the Liao River basin and adjacent Liaodong Bay, China, as well as 10 human/agricultural source samples. Within the 35 river samples, 12 sulfonamides, four acetylated sulfonamides, and trimethoprim were detected, with the dominant being sulfamethox- azole (66.6 ng/L), N-acetylsulfamethoxazole (63.1 ng/L), trimethoprim (29.0 ng/L), sulfadiazine (14.0 ng/L), and sulfamonomethoxine (8.4 ng/L); within the 36 marine samples, 10 chemicals were detected, with the main contributions from sulfamethoxazole (25.2 ng/L) and N-acetylsulfamethoxazole (28.6 ng/L). Sulfamethoxazole (25.9%), N-acetylsulfamethoxazole (46.6%), trimethoprim (22.9%), and sulfapyridine (1.4%) were the main chemicals from human sources, while sulfamonomethoxine, sulfamethazine, sulfaquinoxaline, sulfaguanidine, sulfadiazine, sulfanilamide, and sulfamethoxypyridazine were dominant in the animal husbandry sources, specifically, swine and poultry farms, and sulfamethoxazole (91%) was dominant in the mariculture source. A principal component analysis with multiple linear regression was performed to evaluate the source apportionment of total sulfonamides in Liaodong Bay. It was found that animal husbandry contributed 15.2% of total sulfonamides, while human sources contributed 28.5%, and combined human and mariculture sources contributed 56.3%. In addition, the mariculture contribution was 24.1% of total sulfonamides into the sea based on mass flux estimation. The present study is the first report that the environmental levels of sulfonamide metabolites were comparable to the corresponding parents; therefore, we should pay attention to their environmental occurrence. Source apportionment showed human discharge (60.7%) significantly contributed to these antibiotics in Liaodong Bay, which provides important information for environ- mental management. Environ. Toxicol. Chem. 2011;30:1252–1260. # 2011 SETAC Keywords—Sulfonamides Occurrence River water Seawater Source apportionment INTRODUCTION treatment, while sulfadiazine, sulfadimethoxine, sulfametha- A number of studies have highlighted the environmental zine, sulfathiazole, and sulfachloropyridazine are frequently occurrence of antibiotics after their huge usage throughout the used in veterinary medicine [17]. After oral application, world, and scientists are increasingly concerned about the sulfonamides are excreted via urine and are ultimately released induction and spread of antibiotic resistance and their resistant into the aquatic environment through sewage treatment plant genes in response to an increased selective pressure [1,2]. effluent or agricultural runoff. The removal efficiency of these Sulfonamides are a group of synthetic antibiotics that function compounds during wastewater treatment has proven to be poor as competitive antagonists to p-aminobenzoate in the bacterial [18], and relatively high concentrations of sulfonamides have enzymatic synthesis of dihydrofolic acid [3] and are often been ubiquitously detected in surface water samples [19–24]. administered with trimethoprim to potentiate bactericidal While most of these studies often focused on a narrow range effects [4]. However, some studies had found that continuous of sulfonamides (mainly sulfamethoxazole, sulfamethazine, treatment with sulfonamides such as sulfamerazine and and occasionally sulfapyridine and sulfadiazine), 20 to 30 sulfadimethoxine could induce carcinomas [5–7]. In addition, sulfonamides are commercially available and prevalently sulfonamides resistance genes such as sul1, sul2, and sul3 used around the world [25], which is worth noting because have been found in soils and natural rivers [8,9]. Therefore, of their potential abuse. a gene exchange process known as horizontal transfer, proven In addition to the environmental occurrence of sulfonamides, in the laboratory [10–12], may also happen in the environment their metabolites should get more attention. The main metabolic [8], especially under continuous exposure of sulfonamides pathway for sulfonamides is supposed to be N-acetylation [26] [10,13]. as exemplified by sulfamethoxazole (SMX), of which only 15 to Sulfonamides and trimethoprim are the most frequently 25% is present in unchanged parent form and 43% is present as prescribed antibiotics used in human and veterinary medicine N-acetylsulfamethoxazole (NAcSMX) in the urine [27]. The [14] to treat a variety of bacteria, virus, and protozoan infections retransformation of N-acetylated metabolites into sulfonamides [3,15,16], or as animal growth promoters to improve feed can occur in the environment via microbial activities [1,28]. efficiency [17]. Of these sulfonamides, sulfamethoxazole, This phenomenon has been demonstrated by the transformation sulfapyridine, and sulfamerazine are primarily used in human of NAcSMX to SMX in a water-sediment coexisting test system [29] and N-acetylsulfamethazine to its active parent sulfamethazine during the storage of manure [30]. Thus, sulfo- All Supplemental Data may be found in the online version of this article. namides metabolites are likely to be an extra source of active * To whom correspondence may be addressed sulfonamides within the environment. To our best knowledge, ([email protected]). Published online 23 February 2011 in Wiley Online Library however, only a few studies have focused on the detection (wileyonlinelibrary.com). of NAcSMX in sewage treatment plants [18], while the 1252 Sulfonamides and their metabolites in river and sea samples Environ. Toxicol. Chem. 30, 2011 1253 metabolites of a broad range of sulfonamides in environmental MATERIALS AND METHODS matrices have not been reported. In the present study we developed a liquid chromatography- Chemicals and materials electrospray tandem mass spectrometry (LC-MS/MS) method Sulfaguanidine (SGD), sulfanilamide (SA), sulfathiazole for simultaneously analyzing 19 sulfonamides, five N-acety- (STZ), sulfisomidine (SIM), sulfamonomethoxine (SMM), sul- lated metabolites, and trimethoprim in sewage treatment fisoxazole (SIA), sulfachloropyridazine (SCP), sulfapyridine plant (STP) influent, effluent, and environmental river samples, (SPD), sulfadiazine (SDZ), sulfamethazine (SMA), sulfame- by improving the solid-phase extraction (SPE) cleanup method. thoxazole (SMX), sulfamerazine (SMR), sulfaquinoxaline The method was then applied to investigate the occurrence (SQX), sulfameter (SME), sulfamethizole (SMT), sulfamoxol of target analytes in the Liao River basin, the adjacent Liaodong (SMO), sulfadimethoxine (SDM), sulfamethoxypyridazine Bay, as well as human and agricultural influenced source (SMP), sulfanitran (SNT), and trimethoprim (TMP) were all 13 13 samples in northern China. The parent sulfonamides included obtained from Sigma-Aldrich. C6-sulfamethazine ( C6-SMA) in the present study were chosen because they have potential was obtained from Cambridge Isotope Laboratories. N-acetyl- for use in human medical treatment and animal husbandry in sulfapyridine (NAcSPD), N-acetylsulfadiazine (NAcSDZ), the Liaodong Bay region. Finally, source apportionment N-acetylsulfamethazine (NAcSMA), N-acetylsulfamethoxazole analyses were carried out using principal component (NAcSMX), N-acetylsulfamerazine (NAcSMR), and N-acetylsul- analyses with multiple linear regression based on the profiles famethoxazole-d5 (NAcSMX-d5) were purchased from Toronto of all target compounds to interpret the contribution Research Chemicals (Table 1). from human and agricultural sources to total sulfonamides in The high-performance liquid chromatography (HPLC)- Liaodong Bay. grade methanol, acetone, dichloromethane, ethyl acetate, and Table 1. Chemical structures and electrospray tandem mass spectrometry (ESI-MS/MS) spectra features of target sulfonamides, their metabolites, and trimethoprim a b Compound R1 R2 Mass spectra Compound R1 R2 Mass spectra SGD H 173 (92,156) SQX H 301 (92,156) SA H H 215 (92,156) SME H 281 (92,156) STZ H 256 (92,156) SMT H 271(92,156) SIM H 279 (92,124) SMO H 268 (92,156) SMM H 281 (92,156) SDM H 311 (92,156) SIA H 268 (92,156) SCP H 285 (92,156) SMP H 281 (92,156) SNT 336 (64,156) SDZ H 251 (92,156) NAcSDZ 293 (134,198) SPD H 250 (92,156) NAcSPD 292 (134,198) SMA H 279 (92,186) NAcSMA 281 (92,156) SMX H 254 (92,156) NAcSMX 321 (134,186) SMR H 265 (92,110) NAcSMR 307 (134,172) SAs TMP 291 (110, 123) a SAs ¼ sulfonamide antibiotics; SGD ¼ sulfaguanidine; SA ¼ sulfanilamide; STZ ¼ sulfathiazole; SIM ¼ sulfisomidine; SMM ¼ sulfamonomethoxine; SIA ¼ sulfisoxazole; SMP ¼ sulfamethoxypyridazine; SQX ¼ sulfaquinoxaline; SME ¼ sulfameter; SMT ¼ sulfamethizole; SMO ¼ sulfamoxol; SDM ¼ sulfadimethoxine; SCP ¼ sulfachloropyridazine; SNT ¼ sulfanitran; SDZ ¼ sulfadiazine; NAcSDZ ¼ N-acetylsulfadiazine; SPD ¼ sulfapyridine; NAcSPD ¼ N-acetylsulfapyridine;
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