Environmental Science and Pollution Research

, Volume 24, Issue 30, pp 23771–23782 | Cite as

Electrochemical treatment of penicillin, cephalosporin, and fluoroquinolone antibiotics via active chlorine: evaluation of antimicrobial activity, toxicity, matrix, and their correlation with the degradation pathways

  • Efraím A. Serna-Galvis
  • Karen E. Berrio-Perlaza
  • Ricardo A. Torres-Palma
Research Article

Abstract

Antibiotics are pharmaceuticals widely consumed and frequently detected in environmental water, where they can induce toxic effects and development of resistant bacteria. Their structural variety makes the problem of antibiotics in natural water more complex. In this work, six highly used antibiotics (at 40 μmol L−1) belonging to three different classes (penicillins, cephalosporins, and fluoroquinolones) were treated using an electrochemical system with a Ti/IrO2 anode and a Zr cathode in the presence of NaCl (0.05 μmol L−1). The attack of electrogenerated active chlorine was found to be the main degradation route. After only 20 min of treatment, the process decreased more than 90% of the initial concentration of antibiotics, following the degradation order: fluoroquinolones > penicillins > cephalosporins. The primary interactions of the degrading agent with fluoroquinolones occurred at the cyclic amine (i.e., piperazyl ring) and the benzene ring. Meanwhile, the cephalosporins and penicillins were initially attacked on the β-lactam and sulfide groups. However, the tested penicillins presented an additional reaction on the central amide. In all cases, the transformations of antibiotics led to the antimicrobial activity decreasing. On the contrary, the toxicity level showed diverse results: increasing, decreasing, and no change, depending on the antibiotic type. In fact, due to the conservation of quinolone nucleus in the fluoroquinolone by-products, the toxicity of the treated solutions remained unchanged. With penicillins, the production of chloro-phenyl-isoxazole fragments increased the toxicity level of the resultant solution. However, the opening of β-lactam ring of cephalosporin antibiotics decreased the toxicity level of the treated solutions. Finally, the application of the treatment to synthetic hospital wastewater and seawater containing a representative antibiotic showed that the high amount of chloride ions in seawater accelerates the pollutant degradation. In contrast, the urea and ammonium presence in the hospital wastewater retarded the removal of this pharmaceutical.

Keywords

Reactivity to active chlorine DSA anodes Antibiotics removal Water treatment Complex matrices 

Notes

Acknowledgements

The authors thank COLCIENCIAS (Departamento Administrativo de Ciencia, Tecnología e Innovación, Colombia) and Swiss National Foundation for the financial support through the projects “Desarrollo y evaluación de un sistema electroquímico asistido con luz solar para la eliminación de contaminantes emergentes en agua (No. 111565842980)” and “Treatment of the hospital wastewaters in Cote d’Ivoire and in Colombia by advanced oxidation processes (IZ01Z0_ 146919)”, respectively. The authors also thank the biology student Martha Verbel-Olarte for her useful collaboration in the toxicity test development. E.Serna-Galvis thanks COLCIENCIAS for his Ph.D. scholarship (Convocatoria 647 de 2014).

Supplementary material

11356_2017_9985_MOESM1_ESM.docx (421 kb)
ESM 1 (DOCX 406 kb)

References

  1. Amstutz V, Katsaounis A, Kapalka A et al (2012) Effects of carbonate on the electrolytic removal of ammonia and urea from urine with thermally prepared IrO2 electrodes. J Appl Electrochem 42:787–795CrossRefGoogle Scholar
  2. An T, Yang H, Song W et al (2010) Mechanistic considerations for the advanced oxidation treatment of fluoroquinolone pharmaceutical compounds using TiO2 heterogeneous catalysis. J Phys Chem A 114:2569–2575CrossRefGoogle Scholar
  3. Antonin VS, Santos MC, Garcia-segura S, Brillas E (2015) Electrochemical incineration of the antibiotic ciprofloxacin in sulfate medium and synthetic urine matrix. Water Res 83:31–41CrossRefGoogle Scholar
  4. ASTM International (2014) Standard practice for the preparation of substitute ocean water. ASTM Spec Tech Publ 98:2013–2015Google Scholar
  5. Bunn W, Haas B, Deane E, Kleopfer R (1975) Formation of trihalomethanes by chlorination of surface water. Environ Lett 10:205–213CrossRefGoogle Scholar
  6. Burden DA, Oshero N (1998) Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim Biophys Acta 1400:149–154Google Scholar
  7. Chen G, Li M, Liu X (2015) Fluoroquinolone antibacterial agent contaminants in soil/groundwater: a literature review of sources, fate, and occurrence. Water Air Soil Pollut 226:418CrossRefGoogle Scholar
  8. Clayden J, Greeves N, Warren S, Wothers P (2001) Saturated heterocycles and stereoelectronics. In: Organic chemistry, First. Oxford University Press, New York, pp 1121–1126Google Scholar
  9. Coledam DAC, Aquino JM, Silva BF et al (2016) Electrochemical mineralization of norfloxacin using distinct boron-doped diamond anodes in a filter-press reactor, with investigations of toxicity and oxidation by-products. Electrochim Acta 213:856–864CrossRefGoogle Scholar
  10. Coledam DAC, Pupo MMS, Silva BF et al (2017) Electrochemical mineralization of cephalexin using a conductive diamond anode: a mechanistic and toxicity investigation. Chemosphere 168:638–647CrossRefGoogle Scholar
  11. Comninelis C, Chen G (2010) Electrochemistry for the environment. Springer, LondonCrossRefGoogle Scholar
  12. Cooper R, Koppel G (2014) The chemistry of penicillin sulfoxide. In: Morin RB, Gorman M (eds) Chemistry and biology of B-lactam antibiotics, vol 1. Academic Press, New York, pp 1–88Google Scholar
  13. Corsi C, Volker S, Bobbio C, et al (2011) Isoxazole derivatives for use as fungicides. Patent: EP2365751 A1. Syngenta participations AGGoogle Scholar
  14. Cullen G, Hubbard R (1919) Note on stabilization of dilute sodium hypochlorite solutions (Dakin’s solution). J Biol Chem 37:511–518Google Scholar
  15. Davor S, Pavica S, Tandaric T, Vrcek V (2014) Chlorination of N-methylacetamide and amide-containing pharmaceuticals. Quantum-chemical study of the reaction mechanism. J Phys Chem A 118:2367–2376CrossRefGoogle Scholar
  16. Dbira S, Bensalah N, Cañizares P et al (2015) The electrolytic treatment of synthetic urine using DSA electrodes. J Electroanal Chem 744:62–68CrossRefGoogle Scholar
  17. Deborde M, von Gunten U (2008) Reactions of chlorine with inorganic and organic compounds during water treatment-kinetics and mechanisms: a critical review. Water Res 42:13–51CrossRefGoogle Scholar
  18. Dimitrakopoulou D, Rethemiotaki I, Frontistis Z et al (2012) Degradation, mineralization and antibiotic inactivation of amoxicillin by UV-A/TiO2 photocatalysis. J Environ Manag 98:168–174CrossRefGoogle Scholar
  19. Diwan V, Stalsby C, Tamhankar A (2013) Seasonal and temporal variation in release of antibiotics in hospital wastewater: estimation using continuous and grab sampling. PLoS One 8:e68715CrossRefGoogle Scholar
  20. Dodd MC, Shah AD, Von Gunten U, Huang CH (2005) Interactions of fluoroquinolone antibacterial agents with aqueous chlorine: reaction kinetics, mechanisms, and transformation pathways. Environ Sci Technol 39:7065–7076CrossRefGoogle Scholar
  21. Dodd MC, Rentsch D, Singer HP et al (2010) Transformation of β-lactam antibacterial agents during aqueous ozonation: reaction pathways and quantitative bioassay of biologically-active oxidation products. Environ Sci Technol 44:5940–5948CrossRefGoogle Scholar
  22. Elsea SH, Osheroff N, Nitiss JL (1992) Cytotoxicity of quinolones toward eukaryotic cells: identification of topoisomerase II as the primary cellular target for the quinolone CP-115,953 in yeast. J Biol Chem 267:13150–13153Google Scholar
  23. Frédéric O, Yves P (2014) Pharmaceuticals in hospital wastewater: their ecotoxicity and contribution to the environmental hazard of the effluent. Chemosphere 115:31–39CrossRefGoogle Scholar
  24. Frontistis Z, Antonopoulou M, Venieri D et al (2016) Boron-doped diamond oxidation of amoxicillin pharmaceutical formulation: statistical evaluation of operating parameters, reaction pathways and antibacterial activity. J Environ Manag 195:100–109CrossRefGoogle Scholar
  25. Giraldo AL, Erazo-Erazo ED, Flórez-Acosta OA et al (2015) Degradation of the antibiotic oxacillin in water by anodic oxidation with Ti/IrO2 anodes: evaluation of degradation routes, organic by-products and effects of water matrix components. Chem Eng J 279:103–114CrossRefGoogle Scholar
  26. Githinji LJM, Musey MK, Ankumah RO (2011) Evaluation of the fate of ciprofloxacin and amoxicillin in domestic wastewater. Water Air Soil Pollut 219:191–201CrossRefGoogle Scholar
  27. Gomes de Menezes FL, Cabral da Silva AJ, Martínez-Huitle CA et al (2016) Electrochemical treatment of shrimp farming effluent: role of electrocatalytic material. Environ Sci Pollut Res 24:1–10Google Scholar
  28. Guo H, Gao N, Yang Y, Zhang Y (2016) Kinetics and transformation pathways on oxidation of fluoroquinolones with thermally activated persulfate. Chem Eng J 292:82–91CrossRefGoogle Scholar
  29. Guzmán-Duque FL, Palma-Goyes RE, González I et al (2014) Relationship between anode material, supporting electrolyte and current density during electrochemical degradation of organic compounds in water. J Hazard Mater 278:221–226CrossRefGoogle Scholar
  30. He K, Soares AD, Adejumo H et al (2015) Detection of a wide variety of human and veterinary fluoroquinolone antibiotics in municipal wastewater and wastewater-impacted surface water. J Pharm Biomed Anal 106:136–143CrossRefGoogle Scholar
  31. Homem V, Santos L (2011) Degradation and removal methods of antibiotics from aqueous matrices-a review. J Environ Manag 92:2304–2347CrossRefGoogle Scholar
  32. Hosiner D, Gerber S, Lichtenberg-Fraté H et al (2014) Impact of acute metal stress in Saccharomyces cerevisiae. PLoS One 9:1–14CrossRefGoogle Scholar
  33. Jojoa-Sierra SD, Silva-Agredo J, Herrera-Calderon E, Torres-Palma RA (2017) Elimination of the antibiotic norfloxacin in municipal wastewater, urine and seawater by electrochemical oxidation on IrO2 anodes. Sci Total Environ 575:1228–1238CrossRefGoogle Scholar
  34. Karlesa A, De Vera GAD, Dodd MC et al (2014) Ferrate(VI) oxidation of β-lactam antibiotics: reaction kinetics, antibacterial activity changes, and transformation products. Environ Sci Technol 48:10380–10389CrossRefGoogle Scholar
  35. Khetan SK, Collins TJ (2007) Human pharmaceuticals in the aquatic environment: a challenge to green chemistry. Chem Rev 107:2319–2364CrossRefGoogle Scholar
  36. King DA, Hannum DM, Qi J-S, Hurst JK (2004) HOCl-mediated cell death and metabolic dysfunction in the yeast Saccharomyces cerevisiae. Arch Biochem Biophys 423:170–181CrossRefGoogle Scholar
  37. Konaklieva M (2014) Molecular targets of β-lactam-based antimicrobials: beyond the usual suspects. Antibiotics 3:128–142CrossRefGoogle Scholar
  38. Kümmerer K (2009) Antibiotics in the aquatic environment—a review—part I. Chemosphere 74:417–434CrossRefGoogle Scholar
  39. Larsson DGJ, de Pedro C, Paxeus N (2007) Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J Hazard Mater 148:751–755CrossRefGoogle Scholar
  40. Li L, Wei D, Wei G, Du Y (2013) Transformation of cefazolin during chlorination process: products, mechanism and genotoxicity assessment. J Hazard Mater 262:48–54CrossRefGoogle Scholar
  41. Lin AYC, Yu TH, Lateef SK (2009) Removal of pharmaceuticals in secondary wastewater treatment processes in Taiwan. J Hazard Mater 167:1163–1169CrossRefGoogle Scholar
  42. Mavronikola C, Demetriou M, Hapeshi E et al (2009) Mineralisation of the antibiotic amoxicillin in pure and surface waters by artificial UVA- and sunlight-induced Fenton oxidation. J Chem Technol Biotechnol 84:1211–1217CrossRefGoogle Scholar
  43. Mehta RJ, Nash CH (1978) B-lactamase activity in yeast. J Antibiot 31:239–240CrossRefGoogle Scholar
  44. Neftel KA, Hubscher U (1987) MINIREVIEW effects of B-lactam antibiotics on proliferating eucaryotic cells. Antimicrob Agents Chemother 31:1657–1661CrossRefGoogle Scholar
  45. Niu X-Z, Busetti F, Langsa M, Croué J-P (2016) Roles of singlet oxygen and dissolved organic matter in self-sensitized photo-oxidation of antibiotic norfloxacin under sunlight irradiation. Water Res 106:214–222CrossRefGoogle Scholar
  46. Pattison DI, Davies MJ (2001) Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds. Chem Res Toxicol 14:1453–1464CrossRefGoogle Scholar
  47. Paul T, Dodd MC, Strathmann TJ (2010) Photolytic and photocatalytic decomposition of aqueous ciprofloxacin: transformation products and residual antibacterial activity. Water Res 44:3121–3132CrossRefGoogle Scholar
  48. Rickman KA, Mezyk SP (2010) Kinetics and mechanisms of sulfate radical oxidation of B-lactam antibiotics in water. Chemosphere 81:359–365CrossRefGoogle Scholar
  49. Rumlova L, Dolezalova J (2012) A new biological test utilising the yeast Saccharomyces cerevisiae for the rapid detection of toxic substances in water. Environ Toxicol Pharmacol 33:459–464CrossRefGoogle Scholar
  50. Serna-Galvis EA, Silva-Agredo J, Giraldo-Aguirre AL, Torres-Palma RA (2015) Sonochemical degradation of the pharmaceutical fluoxetine: effect of parameters, organic and inorganic additives and combination with a biological system. Sci Total Environ 524–525:354–360CrossRefGoogle Scholar
  51. Serna-Galvis EA, Silva-Agredo J, Giraldo AL et al (2016a) Comparison of route, mechanism and extent of treatment for the degradation of a β-lactam antibiotic by TiO2 photocatalysis, sonochemistry, electrochemistry and the photo-Fenton system. Chem Eng J 284:953–962CrossRefGoogle Scholar
  52. Serna-Galvis EA, Silva-Agredo J, Giraldo-Aguirre AL et al (2016b) High frequency ultrasound as a selective advanced oxidation process to remove penicillinic antibiotics and eliminate its antimicrobial activity from water. Ultrason Sonochem 31:276–283CrossRefGoogle Scholar
  53. Serna-Galvis EA, Giraldo-Aguirre AL, Silva-Agredo J et al (2017) Removal of antibiotic cloxacillin by means of electrochemical oxidation, TiO2 photocatalysis, and photo-Fenton processes: analysis of degradation pathways and effect of the water matrix on the elimination of antimicrobial activity. Environ Sci Pollut Res 24:6339–6352CrossRefGoogle Scholar
  54. Sirés I, Brillas E (2012) Remediation of water pollution caused by pharmaceutical residues based on electrochemical separation and degradation technologies: a review. Environ Int 40:212–229CrossRefGoogle Scholar
  55. Smaldone G, Marrone R, Cappiello S et al (2014) Occurrence of antibiotic resistance in bacteria isolated from seawater organisms caught in Campania region: preliminary study. BMC Vet Res 10:161CrossRefGoogle Scholar
  56. Sukhdev A, Manjunatha A, Puttaswamy P (2013) Oxidative cleavage of B-lactam ring of cephalosporins with chloramine-T in alkaline medium: a kinetic, mechanistic, and reactivity study. ISRN Phys Chem 2013:1–10CrossRefGoogle Scholar
  57. Szabó L, Tóth T, Engelhardt T et al (2016a) Change in hydrophilicity of penicillins during advanced oxidation by radiolytically generated •OH compromises the elimination of selective pressure on bacterial strains. Sci Total Environ 551–552:393–403CrossRefGoogle Scholar
  58. Szabó L, Tóth T, Rácz G et al (2016b) OH and e-aq are yet good candidates for demolishing the β-lactam system of a penicillin eliminating the antimicrobial activity. Radiat Phys Chem 124:84–90CrossRefGoogle Scholar
  59. TMIC (2016) DrugBank http://www.drugbank.ca/. Accessed 10 Oct 2016
  60. Wang X-H, Lin AY-C (2012) Phototransformation of cephalosporin antibiotics in an aqueous environment results in higher toxicity. Environ Sci Technol 46:12417–12426CrossRefGoogle Scholar
  61. Wang Y, Shen C, Zhang M et al (2016) The electrochemical degradation of ciprofloxacin using a SnO2-Sb/Ti anode: influencing factors, reaction pathways and energy demand. Chem Eng J 296:79–89CrossRefGoogle Scholar
  62. Watkinson AJ, Murby EJ, Kolpin DW, Costanzo SD (2009) The occurrence of antibiotics in an urban watershed: from wastewater to drinking water. Sci Total Environ 407:2711–2723CrossRefGoogle Scholar
  63. Watson K, Shaw G, Leusch FDL, Knight NL (2012) Chlorine disinfection by-products in wastewater effluent: bioassay-based assessment of toxicological impact. Water Res 46:6069–6083CrossRefGoogle Scholar
  64. Xiao R, Ye T, Wei Z et al (2015) Quantitative structure-activity relationship (QSAR) for the oxidation of trace organic contaminants by sulfate radical. Environ Sci Technol 49:13394-13402Google Scholar
  65. Yang H, Liang J, Zhang L, Liang Z (2016) Electrochemical oxidation degradation of methyl orange wastewater by Nb/PbO2 electrode. Int J Electrochem Sci 11:1121–1134Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Efraím A. Serna-Galvis
    • 1
  • Karen E. Berrio-Perlaza
    • 1
  • Ricardo A. Torres-Palma
    • 1
  1. 1.Grupo de Investigación en Remediación Ambiental y Biocatálisis (GIRAB), Instituto de Química, Facultad de Ciencias Exactas y NaturalesUniversidad de Antioquia UdeAMedellínColombia

Personalised recommendations