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Investigation of antibiotics in sea cucumbers: occurrence, pollution characteristics, and human risk assessment

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Abstract

Occurrence and distribution of 24 antibiotics from 7 categories were screened in sea cucumbers (Echinodermata: Holothuroidea) collected from different coastal regions of China. The samples were simultaneously extracted and purified using accelerated solvent extraction with in-cell clean-up and analyzed by ultra-performance liquid chromatography-tandem mass spectrometry. A total of ten antibiotics were detected in the sea cucumbers with concentrations ranging from not detected to 32.8 μg/kg (dry weight). Sulfonamides are predominant antibiotics with a mean concentration of 11.5 μg/kg (dry weight), followed by macrolides (11.3 μg/kg, dry weight) and fluoroquinolones (11.2 μg/kg, dry weight). High concentrations of the antibiotics were found in the samples from the South China Sea, implying that the antibiotic pollution in sea cucumbers was geographical region-dependent, which was further confirmed by principal component analysis. It was also found that the antibiotic levels are slightly higher in instant sea cucumbers than in the dried ones. Hazard quotient calculation suggested no obvious human health risks associated with the consumption of sea cucumbers regarding antibiotics.

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References

  • Alderman DJ, Hastings TS (1998) Antibiotic use in aquaculture: development of antibiotic resistance—potential for consumer health risks. International Journal of Food Science & Technology 33:139–155

    Article  CAS  Google Scholar 

  • Álvarez-Muñoz D, Rodríguez-Mozaz S, Maulvault AL, Tediosi A, Fernández-Tejedor M, Van den Heuvel F, Kotterman M, Marques A, Barceló D (2015) Occurrence of pharmaceuticals and endocrine disrupting compounds in macroalgaes, bivalves, and fish from coastal areas in Europe. Environ Res 143:56–64

    Article  Google Scholar 

  • Barani A, Fallah AA (2015) Occurrence of tetracyclines, sulfonamides, fluoroquinolones and florfenicol in farmed rainbow trout in Iran. Food Agric Immunol 26:420–429

    Article  CAS  Google Scholar 

  • Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144

    Article  CAS  Google Scholar 

  • Cakli S, Cadun A, Kisla D, Dincer T (2004) Determination of quality characteristics of Holothuria tubulosa, (Gmelin, 1788) in Turkish sea (Aegean region) depending on sun drying process step used in Turkey. Journal of Aquatic Food Product Technology 13:69–78

    Article  CAS  Google Scholar 

  • Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, Maxwell S, Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38:1086–1108

    Article  CAS  Google Scholar 

  • Chen H, Liu S, Xu XR, Liu SS, Zhou GJ, Sun KF, Zhao JL, Ying GG (2015) Antibiotics in typical marine aquaculture farms surrounding Hailing Island, South China: occurrence, bioaccumulation and human dietary exposure. Mar Pollut Bull 90:181–187

    Article  CAS  Google Scholar 

  • Cheng D, Liu X, Wang L, Gong W, Liu G, Fu W, Cheng M (2014) Seasonal variation and sediment-water exchange of antibiotics in a shallower large lake in North China. Sci Total Environ 476-477:266–275

    Article  CAS  Google Scholar 

  • Du J, Zhao H, Liu S, Xie H, Wang Y, Chen J (2017) Antibiotics in the coastal water of the South Yellow Sea in China: occurrence, distribution and ecological risks. Sci Total Environ 595:521–527

    Article  CAS  Google Scholar 

  • Farjami B, Nematollahi M, Moradi Y, Nazemi M (2014) Derivation of extracts from Persian Gulf sea cucumber (Holothuria leucospilota) and assessment of its antifungal effect. Iran J Fish Sci 13:785–795

    Google Scholar 

  • Gbylik-Sikorska M, Posyniak A, Mitrowska K, Gajda A, Błądek T, Śniegocki T, Żmudzki J (2014) Occurrence of veterinary antibiotics and chemotherapeutics in fresh water, sediment, and fish of the rivers and lakes in Poland. Bull Vet Inst Pulawy 58:399–404

    Article  CAS  Google Scholar 

  • Hu X, He K, Zhou Q (2012) Occurrence, accumulation, attenuation and priority of typical antibiotics in sediments based on long-term field and modeling studies. J Hazard Mater 225-226:91–98

    Article  CAS  Google Scholar 

  • Kim HY, Lee IS, Oh JE (2017) Human and veterinary pharmaceuticals in the marine environment including fish farms in Korea. Sci Total Environ 579:940–949

    Article  CAS  Google Scholar 

  • Kim J, Park Y, Choi K (2009) Phototoxicity and oxidative stress responses in Daphnia magna under exposure to sulfathiazole and environmental level ultraviolet B irradiation. Aquat Toxicol 91:87–94

    Article  CAS  Google Scholar 

  • Lagesson A, Fahlman J, Brodin T, Fick J, Jonsson M, Byströma P, Klaminder J (2016) Bioaccumulation of five pharmaceuticals at multiple trophic levels in an aquatic food web—insights from a field experiment. Sci Total Environ 568:208–215

    Article  CAS  Google Scholar 

  • Li C, Li H, Guo S, Li X, Zhu X (2015) Evaluation of processing methods on the nutritional quality of sea cucumber (Apostichopus japonicus Selenka). Journal of Aquatic Food Product Technology 4:406–417

    Google Scholar 

  • Li J, Wang T, Shao B, Shen J, Wang S, Wu Y (2012a) Plasmid-mediated quinolone resistance genes and antibiotic residues in wastewater and soil adjacent to swine feedlots: potential transfer to agricultural lands. Environ Health Perspect 120:1144–1149

    Article  CAS  Google Scholar 

  • Li W, Shi Y, Gao L, Liu J, Cai Y (2012b) Investigation of antibiotics in mollusks from coastal waters in the Bohai Sea of China. Environ Pollut 162:56–62

    Article  CAS  Google Scholar 

  • Liu S, Dong G, Zhao H, Chen M, Quan W, Qu B (2018) Occurrence and risk assessment of fluoroquinolones and tetracyclines in cultured fish from a coastal region of northern China. Environ Sci Pollut Res 25:8035–8043

    Article  CAS  Google Scholar 

  • Liu S, Zhao H, Lehmler HJ, Cai X, Chen J (2017a) Antibiotic pollution in marine food webs in Laizhou Bay, North China: trophodynamics and human exposure implication. Environmental Science & Technology 51:2392–2400

    Article  CAS  Google Scholar 

  • Liu X, Steele JC, Meng XZ (2017b) Usage, residue, and human health risk of antibiotics in Chinese aquaculture: a review. Environ Pollut 223:161–169

    Article  CAS  Google Scholar 

  • Liu X, Xue C, Wang Y, Li Z, Xue Y, Xu J (2012) The classification of sea cucumber (Apostichopus japonicus) according to region of origin using multi-element analysis and pattern recognition techniques. Food Control 23:522–527

    Article  CAS  Google Scholar 

  • Luo Y, Xu L, Rysz M, Wang Y, Zhang H, Alvarez PJ (2011) Occurrence and transport of tetracycline, sulfonamide, quinolone, and macrolide antibiotics in the Haihe River Basin, China. Environmental Science & Technology 45:1827–1833

    Article  CAS  Google Scholar 

  • Lv X, Pan L, Wang J, Lu L, Yan W, Zhu Y, Xu Y, Guo M, Zhuang S (2017) Effects of triazole fungicides on androgenic disruption and CYP3A4 enzyme activity. Environ Pollut 222:504–512

    Article  CAS  Google Scholar 

  • Magnusson B & Örnemark U (2014) Eurachem Guide: the fitness for purpose of analytical methods—a laboratory guide to method validation and related topics. ISBN 978-91-87461-59-0. Available from www.eurachem.org

  • Martínez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367

    Article  Google Scholar 

  • McEneff G, Barron L, Kelleher B, Paull B, Quinn B (2014) A year-long study of the spatial occurrence and relative distribution of pharmaceutical residues in sewage effluent, receiving marine waters and marine bivalves. Sci Total Environ 476–477:317–326

    Article  Google Scholar 

  • Robinson AA, Belden JB, Lydy MJ (2005) Toxicity of fluoroquinolone antibiotics to aquatic organisms. Environ Toxicol Chem 24:423–430

    Article  CAS  Google Scholar 

  • Ronquillo MG, Angeles-Hernandez JC (2016) Antibiotic and synthetic growth promoters in animal diets: review of impact and analytical methods. Food Control 72:255–267

    Article  Google Scholar 

  • U.S. Environmental Protection Agency (2000) Guidance for assessing chemical contaminant data for use in fish advisories-risk assessment and fish consumption limits, 3rd edn. Office of Water, Washington, DC

    Google Scholar 

  • Vaccaro E, Giorgi M, Longo V, Mengozzi G, Gervasi PG (2003) Inhibition of cytochrome P450 enzymes by enrofloxacin in the sea bass (Dicentrarchus labrax). Aquat Toxicol 62:27–33

    Article  CAS  Google Scholar 

  • Vragović N, Bažulić D, Njari B (2011) Risk assessment of streptomycin and tetracycline residues in meat and milk on Croatian market. Food Chem Toxicol 49:352–355

    Article  Google Scholar 

  • Song C, Li L, Zhang C, Kamira B, Qiu L, Fan L, Wu W, Meng S, Hu G, Chen J (2017) Occurrence and human dietary assessment of sulfonamide antibiotics in cultured fish around Tai Lake, China. Environ Sci Pollut Res 24:17493–17499

    Article  CAS  Google Scholar 

  • Wei X, Chen J, Xie Q, Zhang S, Li Y, Zhang Y, Xie H (2015) Photochemical behavior of antibiotics impacted by complexation effects of concomitant metals: a case for ciprofloxacin and Cu(II). Environmental Science: Processes & Impacts 17:1220–1227

    CAS  Google Scholar 

  • World Health Organization (WHO) (2014). Antimicrobial resistance: global report on surveillance. Geneva, Switzerland. < http://www.who.int/iris/handle/10665/259744 > ISSN 9789241513449

  • Zhang QQ, Ying GG, Pan CG, Liu YS, Zhao JL (2015) Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environmental Science & Technology 49:6772–6782

    Article  CAS  Google Scholar 

  • Zhang X, Chen S, Xu H, Zhang S, Yan Z, Wang J (2016) Identification and occurrence of endogenous semicarbazide in prawns and crabs from Zhejiang Province, China. Food Additives & Contaminants: Part A 33:252–258

    Google Scholar 

  • Zhao H, Guo W, Quan W, Jiang J, Qu B (2016) Occurrence and levels of nitrofuran metabolites in sea cucumber from Dalian, China. Food Additives & Contaminants: Part A 33:1672–1677

    Article  CAS  Google Scholar 

  • Zhao JL, Liu YS, Liu WR, Jiang YX, Su HC, Zhang QQ, Chen XW, Yang YY, Chen J, Liu SS, Pan CG, Huang GY, Ying GG (2015) Tissue-specific bioaccumulation of human and veterinary antibiotics in bile, plasma, liver and muscle tissues of wild fish from a highly urbanized region. Environ Pollut 198:15–24

    Article  Google Scholar 

  • Zhu M, Zhao H, Xia D, Du J, Xie H, Chen J (2018) Determination of 21 antibiotics in sea cucumber using accelerated solvent extraction with in-cell clean-up coupled to ultra-performance liquid chromatography-tandem mass spectrometry. Food Chem 258:87–94

    Article  CAS  Google Scholar 

  • Zhu YG, Zhao Y, Li B, Huang CL, Zhang SY, Yu S, Yu S, Chen YS, Zhang T, Gillings MR, Su JQ (2017) Continental-scale pollution of estuaries with antibiotic resistance genes. Nature Microbiology 2:1–7

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (No. 21661142001).

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Authors and Affiliations

  1. Key Laboratory of Industrial Ecology and Environmental Engineering (MOE), School of Environmental Science and Technology, Dalian University of Technology, Dalian, 116024, China

    Minghua Zhu, Hongxia Zhao, Jingwen Chen, Huaijun Xie & Juan Du

Authors
  1. Minghua Zhu
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  2. Hongxia Zhao
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  3. Jingwen Chen
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  4. Huaijun Xie
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  5. Juan Du
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Corresponding authors

Correspondence to Hongxia Zhao or Jingwen Chen.

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Responsible editor: Philippe Garrigues

Electronic supplementary material

ESM 1

See Supplementary Material for 1) Parameters of the optimized UPLC-MS/MS method; 2) Recovery and RSD of target compounds; 3) Profiles of the detected antibiotics; 4) Sampling locations; 5) Chromatogram of detected antibiotics. (DOCX 3364 kb)

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Zhu, M., Zhao, H., Chen, J. et al. Investigation of antibiotics in sea cucumbers: occurrence, pollution characteristics, and human risk assessment. Environ Sci Pollut Res 25, 32081–32087 (2018). https://doi.org/10.1007/s11356-018-3131-7

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