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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

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2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2019, Vol. 13 Issue (3) : 39    https://doi.org/10.1007/s11783-019-1123-6
RESEARCH ARTICLE
Analysis of antibiotic resistance of Escherichia coli isolated from the Yitong River in North-east China
Yangyang Yu, Xiaolin Zhu, Guanlan Wu, Chengzhi Wang, Xing Yuan()
School of Environment, Northeast Normal University, Changchun 130117, China
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Abstract

The concentrations of four types of antibiotics in the Yitong River were detected.

The concentration of total coliforms in summer was higher than that in spring.

There was a seasonal difference in antibiotic resistance of E. coli.

The E. coli in the Yitong River was found to have multiple antibiotic resistance.

The Yitong River is one of the largest secondary tributaries of the Songhua River. The area where the Yitong River flows is densely populated and contains the livestock and poultry breeding areas of north-east China. These areas introduce a high risk of antibiotic contamination. In this study, the concentrations of four types of typical antibiotics including quinolones, tetracyclines, sulfonamides, and trimethoprim were determined by solid phase extraction-high performance liquid chromatography. The antibiotic resistance of Escherichia coli caused by antibiotic pollution was investigated. The concentration of total coliforms in the Yitong River was detected by the plate counting method. The antibiotic resistance of E. coli to quinolones, tetracyclines, sulfonamides, and trimethoprim was analyzed by the Kirby-Bauer method. The results showed that the concentration of total coliforms in the summer was higher than that in the spring. There was a seasonal difference in the resistance rate of E. coli to antibiotics except trimethoprim. The antibiotic resistance to fluoroquinolones was relatively low. The resistance rate to tetracyclines was higher during the summer. Moreover, resistance to several antibiotics was observed in all sections. This study provides basic data for research on pollution characteristics and prevention of antibiotic exposure in rivers.

Keywords Yitong River      Coliform bacteria      Antibiotic resistance      Escherichia coli     
Corresponding Author(s): Xing Yuan   
Issue Date: 11 June 2019
 Cite this article:   
Yangyang Yu,Xiaolin Zhu,Guanlan Wu, et al. Analysis of antibiotic resistance of Escherichia coli isolated from the Yitong River in North-east China[J]. Front. Environ. Sci. Eng., 2019, 13(3): 39.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1123-6
https://academic.hep.com.cn/fese/EN/Y2019/V13/I3/39
Fig.1  Sampling sites on the Yitong River.
Antibiotic Susceptible (S) Intermediate (I) Resistant (R)
Ofloxacin 16 13–15 ≤12
Ciprofloxacin a) 21 16–20 ≤15
Sulfisoxazole 17 13–16 ≤12
Tetracycline 15 12–14 ≤11
Trimethoprim 16 11–15 ≤10
Tab.1  Zone diameter interpretative standard for testing antibiotic resistance (Unit: mm)
Antibiotic Water sample a) Sediment sample b)
Detection rate (%) Concentration range (µg/L) Average value (µg/L) Detection rate (%) Concentration range (ng/g) Average value (ng/g)
Ofloxacin 62.50 nd c)–1,361 0.479 0 nd nd
Ciprofloxacin 45.83 nd–0.615 0.312 12.5 nd–20.0 20.0
Oxytetracycline 4.16 nd–0.024 0.024 12.5 nd–9.25 9.25
Tetracycline hydrochloride 8.33 nd–0.266 0.264 0 nd nd
Sulfadiazine 37.50 nd–0.439 0.341 50 nd–5.875 3.229
Sulfamerazine 29.16 nd–1.083 0.387 0 nd nd
Sulfamethazine 4.16 nd–0.387 0.205 37.5 nd–19.825 9.904
Sulfamethoxazole 20.83 nd–0.551 0.153 12.5 nd–56.487 56.487
Trimethoprim 33.33 nd–0.393 0.209 0 nd nd
Tab.2  Concentrations of different antibiotics in eight sections of the Yitong River
Fig.2  The concentration of total coliforms in the Yitong River.
Fig.3  Antibiotic resistance of E. coli in the Yitong River.
Sampling section August 2016 November 2016 May 2017 Average value
S1 40.0 57.2 25.0 40.7
S2 45.0 25.0 44.0 38.0
S3 50.0 20.0 4.0 24.7
S4 15.0 21.7 8.7 15.1
S5 40.0 19.0 25.0 28.0
S6 50.0 35.0 16.7 33.9
S7 70.0 18.0 9.5 32.5
S8 70.0 37.5 27.3 44.9
Tab.3  Multiple antibiotic resistance rate of E. coli (Unit: %)
1 F Al-Badaii, M Shuhaimi-Othman (2015). Water pollution and its impact on the prevalence of antibiotic-resistant E. coli and total coliform bacteria: a study of the Semenyih River, Peninsular Malaysia. Water Quality, Exposure and Health, 7(3): 319–330
https://doi.org/10.1007/s12403-014-0151-5
2 L Chidamba, E Cilliers, C C Bezuidenhout (2016). Spatial and temporal variations in pollution indicator bacteria in the Lower Vaal River, South Africa. Water Environment Research, 88(11): 2142–2149
https://doi.org/10.2175/106143016X14733681695528 pmid: 28661330
3 CLSI (2013). Performance standards for antimicrobial susceptibility testing; Twenty-second informational supplement. CLSI document M100–S23. Wayne, PA: Clinical and Laboratory Standards Institute
4 I M Cullen, R P Manecksha, E McCullagh, S Ahmad, F O’Kelly, R Flynn, T E McDermott, P Murphy, R Grainger, J P Fennell, J A Thornhill (2013). An 11-year analysis of the prevalent uropathogens and the changing pattern of Escherichia coli antibiotic resistance in 38,530 community urinary tract infections, Dublin 1999–2009. Irish Journal of Medical Science, 182(1): 81–89
https://doi.org/10.1007/s11845-012-0834-5 pmid: 22669684
5 T F B X da Silva, D T Ramos, M Dziedzic, C M R de Oliveira , E C de Vasconcelos (2011). Microbiological quality and antibiotic resistance analysis of a brazilian water supply source. Water, Air, and Soil Pollution, 218(1–4): 611–618
https://doi.org/10.1007/s11270-010-0672-x
6 D Dong, L Zhang, S Liu, Z Guo, X Hua (2016). Antibiotics in water and sediments from Liao River in Jilin Province, China: Occurrence, distribution, and risk assessment. Environmental Earth Sciences, 75(16): 1202
https://doi.org/10.1007/s12665-016-6008-4
7 J Du, H Zhao, S Liu, H Xie, Y Wang, J Chen (2017). Antibiotics in the coastal water of the South Yellow Sea in China: Occurrence, distribution and ecological risks. Science of the Total Environment, 595: 521–527
https://doi.org/10.1016/j.scitotenv.2017.03.281 pmid: 28395267
8 M S Fram, K Belitz (2011). Occurrence and concentrations of pharmaceutical compounds in groundwater used for public drinking-water supply in California. Science of the Total Environment, 409(18): 3409–3417
https://doi.org/10.1016/j.scitotenv.2011.05.053 pmid: 21684580
9 L Gao, Y Shi, W Li, H Niu, J Liu, Y Cai (2012). Occurrence of antibiotics in eight sewage treatment plants in Beijing, China. Chemosphere, 86(6): 665–671
https://doi.org/10.1016/j.chemosphere.2011.11.019 pmid: 22154158
10 E A Gilroy, J S Klinck, S D Campbell, R McInnis, P L Gillis, S R de Solla (2014). Toxicity and bioconcentration of the pharmaceuticals moxifloxacin, rosuvastatin, and drospirenone to the unionid mussel Lampsilis siliquoidea. Science of the Total Environment, 487: 537–544
https://doi.org/10.1016/j.scitotenv.2014.03.051 pmid: 24813769
11 M González-Pleiter, S Gonzalo, I Rodea-Palomares, F Leganés, R Rosal, K Boltes, E Marco, F Fernández-Piñas (2013). Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: Implications for environmental risk assessment. Water Research, 47(6): 2050–2064
https://doi.org/10.1016/j.watres.2013.01.020 pmid: 23399078
12 A Gulkowska, H W Leung, M K So, S Taniyasu, N Yamashita, L W Yeung, B J Richardson, A P Lei, J P Giesy, P K S Lam (2008). Removal of antibiotics from wastewater by sewage treatment facilities in Hong Kong and Shenzhen, China. Water Research, 42(1–2): 395–403
https://doi.org/10.1016/j.watres.2007.07.031 pmid: 17706267
13 S Guyomard-Rabenirina, C Dartron, M Falord, S Sadikalay, C Ducat, V Richard, S Breurec, O Gros, A Talarmin (2017). Resistance to antimicrobial drugs in different surface waters and wastewaters of Guadeloupe. PLoS One, 12(3): e0173155
https://doi.org/10.1371/journal.pone.0173155 pmid: 28253356
14 B Halling-Sørensen, S Nors Nielsen, P F Lanzky, F Ingerslev, H C Holten Lützhøft, S E Jørgensen (1998). Occurrence, fate and effects of pharmaceutical substances in the environment: A review. Chemosphere, 36(2): 357–393
https://doi.org/10.1016/S0045-6535(97)00354-8 pmid: 9569937
15 M Hawkes, M Barton, J Conly, L Nicolle, C Barry, E L Ford-Jones (2007). Community-associated MRSA: Superbug at our doorstep. Canadian Medical Association Journal, 176(1): 54–56
https://doi.org/10.1503/cmaj.061370 pmid: 17200391
16 X He, M Deng, Q Wang, Y Yany, Y Yang, X Nie (2016). Residues and health risk assessment of quinolones and sulfonamides in cultured fish from Pearl River Delta, China. Aquaculture, 458: 38–46
https://doi.org/10.1016/j.aquaculture.2016.02.006
17 Y Hu, X Yan, Y Shen, M Di, J Wang (2018). Antibiotics in surface water and sediments from Hanjiang River, Central China: Occurrence, behavior and risk assessment. Ecotoxicology and Environmental Safety, 157: 150–158
https://doi.org/10.1016/j.ecoenv.2018.03.083 pmid: 29621706
18 A Jia, Y Wan, Y Xiao, J Hu (2012). Occurrence and fate of quinolone and fluoroquinolone antibiotics in a municipal sewage treatment plant. Water Research, 46(2): 387–394
https://doi.org/10.1016/j.watres.2011.10.055 pmid: 22118907
19 G Kim, E Choi, D Lee (2005). Diffuse and point pollution impacts on the pathogen indicator organism level in the Geum River, Korea. Science of the Total Environment, 350(1–3): 94–105
https://doi.org/10.1016/j.scitotenv.2005.01.021 pmid: 16227076
20 J W Kim, H Ishibashi, R Yamauchi, N Ichikawa, Y Takao, M Hirano, M Koga, K Arizono (2009). Acute toxicity of pharmaceutical and personal care products on freshwater crustacean (Thamnocephalus platyurus) and fish (Oryzias latipes). The Journal of Toxicological Sciences, 34(2): 227–232
https://doi.org/10.2131/jts.34.227 pmid: 19336980
21 S C Kim, K Carlson (2007). Temporal and spatial trends in the occurrence of human and veterinary antibiotics in aqueous and river sediment matrices. Environmental Science & Technology, 41(1): 50–57
https://doi.org/10.1021/es060737+ pmid: 17265926
22 Y Kim, K B Lee, K Choi (2016). Effect of runoff discharge on the environmental levels of 13 veterinary antibiotics: A case study of Han River and Kyungahn Stream, South Korea. Marine Pollution Bulletin, 107(1): 347–354
https://doi.org/10.1016/j.marpolbul.2016.03.011 pmid: 27016960
23 T X Le, Y Munekage (2004). Residues of selected antibiotics in water and mud from shrimp ponds in mangrove areas in Viet Nam. Marine Pollution Bulletin, 49(11–12): 922–929
https://doi.org/10.1016/j.marpolbul.2004.06.016 pmid: 15556177
24 S Li, W Shi, H Li, N Xu, R Zhang, X Chen, W Sun, D Wen, S He, J Pan, Z He, Y Fan (2018). Antibiotics in water and sediments of rivers and coastal area of Zhuhai City, Pearl River estuary, south China. Science of the Total Environment, 636: 1009–1019
https://doi.org/10.1016/j.scitotenv.2018.04.358 pmid: 29913564
25 X Liang, B Chen, X Nie, Z Shi, X Huang, X Li (2013). The distribution and partitioning of common antibiotics in water and sediment of the Pearl River Estuary, south China. Chemosphere, 92(11): 1410–1416
https://doi.org/10.1016/j.chemosphere.2013.03.044 pmid: 23628172
26 J Liu, G Lu, D Wu, Z Yan (2014). A multi-biomarker assessment of single and combined effects of norfloxacin and sulfamethoxazole on male goldfish (Carassius auratus). Ecotoxicology and Environmental Safety, 102: 12–17
https://doi.org/10.1016/j.ecoenv.2014.01.014 pmid: 24580816
27 Q, Liu M, Li X, Liu Q, Zhang R, Liu Z Wang , X, Shi J, Quan X, Shen F Zhang (2018). Removal of sulfamethoxazole and trimethoprim from reclaimed water and the biodegradation mechanism. Frontiers of Environmental Science & Engineering, 12(6): 6
28 A Łuczkiewicz, K Jankowska, S Fudala-Książek, K Olańczuk-Neyman (2010). Antimicrobial resistance of fecal indicators in municipal wastewater treatment plant. Water Research, 44(17): 5089–5097
https://doi.org/10.1016/j.watres.2010.08.007 pmid: 20810144
29 P Martins da Costa, P Vaz-Pires, F Bernardo (2006). Antimicrobial resistance in Enterococcus spp. isolated in inflow, effluent and sludge from municipal sewage water treatment plants. Water Research, 40(8): 1735–1740
https://doi.org/10.1016/j.watres.2006.02.025 pmid: 16603222
30 A Morris, J D Kellner, D E Low (1998). The superbugs: Evolution, dissemination and fitness. Current Opinion in Microbiology, 1(5): 524–529
https://doi.org/10.1016/S1369-5274(98)80084-2 pmid: 10066531
31 M Pan, L M Chu (2018). Occurrence of antibiotics and antibiotic resistance genes in soils from wastewater irrigation areas in the Pearl River Delta region, southern China. Science of the Total Environment, 624: 145–152
https://doi.org/10.1016/j.scitotenv.2017.12.008 pmid: 29258031
32 M G Pintadoherrera, C Wang, J Lu, Y Chang, W Chen, X Li, P A Lara-Martín (2017). Distribution, mass inventories, and ecological risk assessment of legacy and emerging contaminants in sediments from the Pearl River Estuary in China. Journal of Hazardous Materials, 323 (Pt A): 128–138
33 F Pouzaud, M Dutot, C Martin, M Debray, J M Warnet, P Rat (2006). Age-dependent effects on redox status, oxidative stress, mitochondrial activity and toxicity induced by fluoroquinolones on primary cultures of rabbit tendon cells. Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology, 143(2): 0–241
34 F Riva, E Zuccato, S Castiglioni (2015). Prioritization and analysis of pharmaceuticals for human use contaminating the aquatic ecosystem in Italy. Journal of Pharmaceutical and Biomedical Analysis, 106: 71–78
https://doi.org/10.1016/j.jpba.2014.10.003 pmid: 25459268
35 P H Roberts, K V Thomas (2006). The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchment. Science of the Total Environment, 356(1–3): 143–153
https://doi.org/10.1016/j.scitotenv.2005.04.031 pmid: 15936058
36 M Seoane, C Rioboo, C Herrero, Á Cid (2014). Toxicity induced by three antibiotics commonly used in aquaculture on the marine microalga Tetraselmis suecica (Kylin) Butch. Marine Environmental Research, 101: 1–7
https://doi.org/10.1016/j.marenvres.2014.07.011 pmid: 25150445
37 X, SongR, Liu L, Chen T Kawagishi(2017). Comparative experiment on treating digested piggery wastewater with a biofilm MBR and conventional MBR: Simultaneous removal of nitrogen and antibiotics. Frontiers of Environmental Science & Engineering, 11(2): 11
38 L Wollenberger, B Halling-Sørensen, K O Kusk (2000). Acute and chronic toxicity of veterinary antibiotics to Daphnia magna. Chemosphere, 40(7): 723–730
https://doi.org/10.1016/S0045-6535(99)00443-9 pmid: 10705550
39 D Wu, Z Huang, K Yang, D Graham, B Xie (2015). Relationships between antibiotics and antibiotic resistance gene levels in municipal solid waste leachates in Shanghai, China. Environmental Science & Technology, 49(7): 4122–4128
https://doi.org/10.1021/es506081z pmid: 25760223
40 M H Wu, C J Que, G Xu, Y F Sun, J Ma, H Xu, R Sun, L Tang (2016). Occurrence, fate and interrelation of selected antibiotics in sewage treatment plants and their receiving surface water. Ecotoxicology and Environmental Safety, 132: 132–139
https://doi.org/10.1016/j.ecoenv.2016.06.006 pmid: 27318556
41 X L Wu, L Xiang, Q Y Yan, Y N Jiang, Y W Li, X P Huang, H Li, Q Y Cai, C H Mo (2014). Distribution and risk assessment of quinolone antibiotics in the soils from organic vegetable farms of a subtropical city, southern China. Science of the Total Environment, 487(1): 399–406
pmid: 24797736
42 H Xiao (2014). Pharmacokinetic of Compound Sulfadiazine in GIFT. Dissertation for the Master Degree. Shanghai: Shanghai Ocean University (in Chinese)
43 W Xu, G Zhang, X Li, S Zou, P Li, Z Hu, J Li (2007). Occurrence and elimination of antibiotics at four sewage treatment plants in the Pearl River Delta (PRD), South China. Water Research, 41(19): 4526–4534
https://doi.org/10.1016/j.watres.2007.06.023 pmid: 17631935
44 L Yao, Y Wang, L Tong, Y Li, Y Deng, W Guo, Y Gan (2015). Seasonal variation of antibiotics concentration in the aquatic environment: A case study at Jianghan Plain, central China. Science of the Total Environment, 527– 528: 56–64
https://doi.org/10.1016/j.scitotenv.2015.04.091 pmid: 25956148
45 Z Yu, L Jiang, D Yin (2011). Behavior toxicity to Caenorhabditis elegans transferred to the progeny after exposure to sulfamethoxazole at environmentally relevant concentrations. Journal of Environmental Sciences-China, 23(2): 294–300
https://doi.org/10.1016/S1001-0742(10)60436-6 pmid: 21517004
46 S H Zhang, X Lv, B Han, X Gu, P F Wang, C Wang, Z He (2015). Prevalence of antibiotic resistance genes in antibiotic-resistant Escherichia coli isolates in surface water of Taihu Lake Basin, China. Environmental Science and Pollution Research International, 22(15): 11412–11421
https://doi.org/10.1007/s11356-015-4371-4 pmid: 25813640
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