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Environmental Science and Pollution Research

, Volume 20, Issue 6, pp 3592–3606 | Cite as

Investigating the fate of iodinated X-ray contrast media iohexol and diatrizoate during microbial degradation in an MBBR system treating urban wastewater

  • E. Hapeshi
  • A. Lambrianides
  • P. Koutsoftas
  • E. Kastanos
  • C. Michael
  • D. Fatta-KassinosEmail author
Wastewater Reuse Applications and Contaminants of Emerging Concern (WRA & CEC 2012)

Abstract

The capability of a moving bed biofilm reactor (MBBR) to remove the iodinated contrast media (ICM) iohexol (IOX) and diatrizoate (DTZ) from municipal wastewater was studied. A selected number of clones of microorganisms present in the biofilm were identified. Biotransformation products were tentatively identified and the toxicity of the treated effluent was assessed. Microbial samples were DNA-sequenced and subjected to phylogenetic analysis in order to confirm the identity of the microorganisms present and determine the microbial diversity. The analysis demonstrated that the wastewater was populated by a bacterial consortium related to different members of Proteobacteria, Firmicutes, and Nitrisporae. The optimum removal values of the ICM achieved were 79 % for IOX and 73 % for DTZ, whereas 13 biotransformation products for IOX and 14 for DTZ were identified. Their determination was performed using ultra-performance liquid chromatography–tandem mass spectrometry. The toxicity of the treated effluent tested to Daphnia magna showed no statistical difference compared to that without the addition of the two ICM. The MBBR was proven to be a technology able to remove a significant percentage of the two ICM from urban wastewater without the formation of toxic biodegradation products. A large number of biotransformation products was found to be formed. Even though the amount of clones sequenced in this study does not reveal the entire bacterial diversity present, it provides an indication of the predominating phylotypes inhabiting the study site.

Keywords

Iodinated contrast media Moving bed biofilm reactor Biotransformation products Microbial colonization Toxicity testing 

Notes

Acknowledgments

This work has been implemented within the framework of the project UPGRADING/DURABLE/0308/07, “Fate, Effect and Removal Potential of Xenobiotics Present in Aqueous Matrices (IX-Aqua)” and NIREAS-International Water Research Center activities (project NEA IPODOMI/STRATH/0308/09), both co-funded by the Republic of Cyprus and the European Regional Development Fund through the Research Promotion Foundation of Cyprus.

Supplementary material

11356_2013_1605_MOESM1_ESM.docx (385 kb)
ESM 1 (DOCX 384 kb)

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410Google Scholar
  2. Alfreider A, Vogt C, Babel W (2002) Microbial diversity in an in situ reactor system treating monochlorobenzene contaminated groundwater as revealed by 16S ribosomal DNA analysis. Syst Appl Microbiol 25(2):232–240CrossRefGoogle Scholar
  3. Alfreider A, Vogt C (2007) Bacterial diversity and aerobic biodegradation potential in a BTEX-contaminated aquifer. Water Air Soil Pollut 183:415–426CrossRefGoogle Scholar
  4. Andreottola G, Foladori P, Ragazzi M, Tatàno F (2000) Experimental comparison between MBBR and activated sludge system for the treatment of municipal wastewater. Water Sci Technol 41:375–382Google Scholar
  5. Benotti MJ, Stanford BD, Wert EC, Snyder SA (2009) Evaluation of a photocatalytic reactor membrane pilot system for the removal of pharmaceuticals and endocrine disrupting compounds from water. Water Res 43(6):1513–1522CrossRefGoogle Scholar
  6. Blake MP, Halasz SJ (1995) The effects of X-ray contrast media on bacterial growth. Australas Radiol 39(1):10–13CrossRefGoogle Scholar
  7. Busetti F, Linge KL, Blythe JW, Heitz A (2008) Rapid analysis of iodinated X-ray contrast media in secondary and tertiary wastewater by direct injection liquid chromatography–tandem mass spectrometry. J Chromatogr A 1213(2):200–208CrossRefGoogle Scholar
  8. Calderón K, Martín-Pascual J, Poyatos MJ, Rodelas B, González-Martínez A, González-López J (2012) Comparative analysis of the bacterial diversity in a lab-scale moving bed biofilm reactor (MBBR) applied to treat urban wastewater under different operational conditions. Biores Technol 121:119–126CrossRefGoogle Scholar
  9. Carballa M, Omil F, Lema MJ, Llompart M, García-Jares C, Rodríguez I, Gómez M, Ternes T (2004) Behavior of pharmaceuticals, cosmetics and hormones in a sewage treatment plant. Water Res 38:2918–2926CrossRefGoogle Scholar
  10. Delnavaz M, Ayati B, Ganjidoust (2010) Prediction of moving bed biofilm reactor (MBBR) performance for the treatment of aniline using artificial neural networks (ANN). J Hazard Mater 179:769–775CrossRefGoogle Scholar
  11. Doll TE, Frimmel FH (2005) Removal of selected persistent organic pollutants by heterogeneous photocatalysis in water. Catal Today 101:195–202CrossRefGoogle Scholar
  12. Doll TE, Frimmel FH (2004) Kinetic study of photocatalytic degradation of carbamazepine, clofibric acid, iomeprol and iopromide assisted by different TiO2 materials—determination of intermediates and reaction pathways. Water Res 38(4):955–964CrossRefGoogle Scholar
  13. Doll TE, Frimmel FH (2003) Fate of pharmaceuticals—photodegradation by simulated solar UV-light. Chemosphere 52:1757–1769CrossRefGoogle Scholar
  14. Drewes JE, Fox P, Jekel M (2001) Occurrence of iodinated X-ray contrast media in domestic effluents and their fate during indirect potable reuse. J Environ Sci Health 36(9):1633–1645CrossRefGoogle Scholar
  15. Ferrai M, Guglielmi G, Andreottola G (2010) Modelling respirometric tests for the assessment of kinetic and stoichiometric parameters on MBBR biofilm for municipal wastewater treatment. Environm Modell Softw 25:626–632CrossRefGoogle Scholar
  16. Fono LJ, Sedlak DL (2007) A simple method for the measurement of organic iodine in wastewater and surface water. Water Res 41:1580–1586CrossRefGoogle Scholar
  17. Gapes DJ, Keller J (2009) Impact of oxygen mass transfer on nitrification reactions in suspended carrier reactor biofilms. Process Biochem 44:43–53CrossRefGoogle Scholar
  18. Gartiser S, Brinker L, Erbe T, Kümmerer K, Willmund R (1996) Belastung von Krankenhausabwasser mit gefährlichen Stoffen im Sinne § 7a WHG. Acta Hydrochim Hydrobiol 24(2):90–97CrossRefGoogle Scholar
  19. Haiß A, Kümmerer K (2006) Biodegradability of the X-ray contrast compound diatrizoic acid, identification of aerobic degradation products and effects against sewage sludge micro-organisms. Chemosphere 62:294–302CrossRefGoogle Scholar
  20. Häggblom M (1990) Mechanisms of bacterial degradation and transformation of chlorinated monoaromatic compounds. J Basic Microbiol 30:115–141CrossRefGoogle Scholar
  21. Hem L, Rusten B, Odegaard H (1994) Nitrification in a moving bed reactor. Water Res 28:1425–1433CrossRefGoogle Scholar
  22. Hennebel T, De Corte S, Vanhaecke L, Vanherck K, Forrez I, De Gusseme B, Verhagen P, Verbeken K, van der Bruggen B, Vankelecom I, Nico Boon N, Willy V (2010) Removal of diatrizoate with catalytically active membranes incorporating microbially produced palladium nanoparticles. Water Res 44:1498–1506CrossRefGoogle Scholar
  23. Hirsch R, Ternes TA, Lindart A, Haberer K, Wilken RD (2000) A sensitive method for the determination of iodine containing diagnostic agents in aqueous matrices using LC–electrospray–tandem-MS detection. Fresenius J Anal Chem 366(8):835–841CrossRefGoogle Scholar
  24. Hosseini SH, Borghei SM (2005) The treatment of phenolic wastewater using a moving bed bio-reactor. Process Biochem 40:1027–1030CrossRefGoogle Scholar
  25. Huber MM, Göbel A, Joss A, Hermann N, Löffler D, McArdell CS, Ried A, Siegrist H, Ternes TA, von Gunten U (2005) Oxidation of pharmaceuticals during ozonation of municipal wastewater effluents: a pilot study. Environ Sci Technol 39(11):4290–4299CrossRefGoogle Scholar
  26. Jeong J, Jung J, Cooper WJ, Song W (2010) Degradation mechanisms and kinetic studies for the treatment of X-ray contrast media compounds by advanced oxidation/reduction processes. Water Res 44:4391–4398CrossRefGoogle Scholar
  27. Joss A, Zabczynski S, Göbel A, Hoffmann B, Löffler D, McArdell CS, Ternes TA, Thomsen A, Siegrist H (2006) Biological degradation of pharmaceuticals in municipal wastewater treatment: proposing a classification scheme. Water Res 40(8):1686–1696CrossRefGoogle Scholar
  28. Kalsch W (1999) Biodegradation of the iodinated X-ray contrast media diatrizoate and iopromide. Sci Total Environ 225:143–153CrossRefGoogle Scholar
  29. Khan DJ, Ilyas S, Javid S, Visvanathan C, Jegatheesan V (2011) Performance of suspended and attached growth MBR systems in treating high strength synthetic wastewater. Biores Technol 102(2):5331–5336CrossRefGoogle Scholar
  30. Köhler C, Venditti S, Igos E, Klepiszawski K, Benetto E, Cornelissen A (2012) Elimination of pharmaceutical residues in biologically pre-treated hospital wastewater using advanced UV irradiation technology: a comparative assessment. J Hazard Mater 239–240:70–77CrossRefGoogle Scholar
  31. Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans ADL, van Elsas JD (eds) (2004) Molecular microbial ecology manual, 2nd edn. Kluwer, Dordrecht, the NetherlandsGoogle Scholar
  32. Kunkel U, Radke M (2008) Biodegradation of acidic pharmaceuticals in bed sediments: insight from a laboratory experiment. Environ Sci Technol 42(19):7273–7279CrossRefGoogle Scholar
  33. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  34. Lei G, Ding L, Wang F, Zhang X (2010) A full-scale biological treatment system application in the treated wastewater of pharmaceutical industrial park. Biores Technol 101:5852–5861CrossRefGoogle Scholar
  35. H-Q L, Han H-J D, M-A WW (2011) Removal of phenols, thiocyanate and ammonium from coal gasification wastewater using moving bed biofilm reactor. Biores Technol 102:4667–4673CrossRefGoogle Scholar
  36. Lim YW, Lee SA, Kim SB, Yong HY, Yeon SH, Park YK, Jeong DW, Park JS (2005) Diversity of denitrifying bacteria isolated from Daejeon sewage treatment plant. J Microbiol 43(5):383–390Google Scholar
  37. Loukidou MX, Zouboulis AI (2001) Comparison of two biological treatment processes using attached-growth biomass for sanitary landfill leachate treatment. Environ Pollut 111:273–281CrossRefGoogle Scholar
  38. Mao Y, Schoneich C, Asmus K-D (1991) Identification of organic acids and other intermediates in oxidative degradation of chlorinated ethanes on TiO2, surfaces en route to mineralization. A combined photocatalytic and radiation chemical study. J Phys Chem 95:10080–10089CrossRefGoogle Scholar
  39. McQuarrie JP, Boltz JP (2011) Moving bed biofilm reactor technology: process applications, design, and performance. Water Environ Res 83:560–575CrossRefGoogle Scholar
  40. Messing J, Vieira J, Yanish-Perron C (1984) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:102–119Google Scholar
  41. Mohn WW, Tiedje JM (1992) Microbial reductive dehalogenation. Microbiol Rev 56:482–507Google Scholar
  42. Mönig J, Asmus K-D (1984) One-electron reduction of halothane (2-bromo-2-chloro-l,1,1-trifluoroethane) by free radicals. Radiation chemical model system for reductive metabolism. J Chem Soc Perkin Trans 2:2057–2063Google Scholar
  43. Mönig J, Bahneman D, Asmus K-D (1983a) One-electron reduction of CCl4 in oxygenated aqueous solutions: a CCl3O2-free radical mediated formation of Cl and CO2. Chem Biol Interact 45:15–27CrossRefGoogle Scholar
  44. Mönig J, Krischer K, Asmus K-D (1983b) One-electron reduction of halothane and formation of halide ions in aqueous solutions. Chem Biol Interact 45:43–52CrossRefGoogle Scholar
  45. Ødegaard H (2006) Innovations in wastewater treatment: the moving bed biofilm process. Water Sci Technol 53(9):17–33CrossRefGoogle Scholar
  46. Ødegaard H, Rusten B, Westrum TA (1994) New moving bed biofilm reactor—application and results. Proceedings of the 2nd International Specialized Conference on Biofilm Reactors, International Association on Water Quality, London, UK, pp 221–229Google Scholar
  47. Pérez S, Barceló D (2007) Fate and occurrence of X-ray contrast media in the environment. Anal Bioanal Chem 387:1235–1246CrossRefGoogle Scholar
  48. Pérez S, Eichhorn P, Celiz MD, Aga DS (2006) Structural characterization of metabolites of the X-ray contrast agent iopromide in activated sludge using ion trap mass spectrometry. Anal Chem 78(6):1866–1874CrossRefGoogle Scholar
  49. Putschew A, Schittko S, Jekel M (2001) Quantification of triiodinated benzene derivatives and X-ray contrast media in water samples by liquid chromatography–electrospray tandem mass spectrometry. J Chromatogr A 930:127–134CrossRefGoogle Scholar
  50. Rusten B, Matteson E, Broch-Due A, Westrum T (1994) Treatment of pulp and paper industry wastewater in novel moving bed biofilm reactors. Water Sci Technol 30(3):161–171Google Scholar
  51. Schulz M, Löffler WM, Ternes TA (2008) Transformation of the X-ray contrast medium iopromide in soil and biological wastewater treatment. Environ Sci Technol 42:7207–7217CrossRefGoogle Scholar
  52. Seitz W, Weber WH, Jiang JQ, Lloyd BJ, Maier M, Maier D, Schulz W (2006a) Monitoring of iodinated X-ray contrast media in surface water. Chemosphere 64(8):1318–1324CrossRefGoogle Scholar
  53. Seitz W, Jiang JQ, Weber WH, Lloyd BJ, Maier M, Maier D (2006b) Removal of iodinated X-ray contrast media during drinking water treatment. Environ Chem 3(1):35–39CrossRefGoogle Scholar
  54. Seitz W, Jiang J-Q, Schulz W, Walter H, Weber WH, Maier D, Maier M (2008) Formation of oxidation by-products of the iodinated X-ray contrast medium iomeprol during ozonation. Chemosphere 70:1238–1246CrossRefGoogle Scholar
  55. Shore LJ, M’Coy WS, Gunsch KC, Deshusses AM (2012) Application of a moving bed biofilm reactor for tertiary ammonia treatment in high temperature industrial wastewater. Biores Technol 112:51–60CrossRefGoogle Scholar
  56. Sprehe M, Geiβen SU, Vogelpohl A (2001) Photochemical oxidation of iodized X-ray contrast media (XRC) in hospital wastewater. Water Sci Technol 44(5):317–323Google Scholar
  57. Steger-Hartmann T, Länge R, Schweinfurth H, Tschampel M, Rehmann I (2002) Investigations into the environmental fate and effects of iopromide (ultravist), a widely used iodinated X-ray contrast medium. Water Res 36:266–274CrossRefGoogle Scholar
  58. Sugihara MN, Moeller D, Paul T, Strathmann TJ (2013) TiO2-photocatalyzed transformation of the recalcitrant X-ray contrast agent diatrizoate. Appl Catal B: Environ 7129:114–122CrossRefGoogle Scholar
  59. Ternes TA, Stüber J, Herrmann N, McDowell D, Ried A, Kampman M, Teiser B (2003) Ozonation: a tool for removal of pharmaceuticals, contrast media and musk fragrances from wastewater? Water Res 37:1976–1982CrossRefGoogle Scholar
  60. Ternes TA, Hirsch R (2000) Occurrence and behavior of X-ray contrast media in sewage facilities and the aquatic environment. Environ Sci Technol 34:2741–2748CrossRefGoogle Scholar
  61. Torsvik V, Salte K, Sørheim R, Goksøyr J (1990) Comparison of phenotypic diversity and DNA heterogeneity in a population of soil bacteria. Appl Environ Microbiol 56(3):776–81Google Scholar
  62. Trakhna F, Harf-Monteil C, AbdelNour1 A, Maaroufi A, Gadonna-Widehem P (2009) Rapid Aeromonas hydrophila identification by TaqMan PCR assay: comparison with a phenotypic method. Lett Appl Microbiol 49:186–190Google Scholar
  63. Velo-Gala I, López-Peñalver JJ, Sánchez-Polo M, Rivera-Utrilla J (2012) Ionic X-ray contrast media degradation in aqueous solution induced by gamma radiation. Chem Eng J 195–196:369–376CrossRefGoogle Scholar
  64. Wagner M, Amann R, Lemmer H, Schleifer KH (1993) Probing activated sludge with oligonucleotides specific for proteobacteria: inadequacy of culture-dependent methods for describing microbial community structure. Appl Environ Microbiol 59(5):1520–1525Google Scholar
  65. Weiss JS, Alvarez M, Tang C, Horvath RW, Stahl JF (2005) Evaluation of moving bed biofilm reactor technology for enhancing nitrogen removal in a stabilization pond treatment plant. Proceedings of the 78th Annual Water Environment Federation Technical Exposition and Conference, Washington, DC, October 29–November 2. Water Environ Federation, Alexandria, Virginia, pp 3889–3904Google Scholar
  66. Wéry N, Monteil C, Pourcher AM, Godon JJ (2010) Human-specific fecal bacteria in wastewater treatment plant effluents. Water Res 44(6):1873–1883CrossRefGoogle Scholar
  67. Zupanc M, Kosjek T, Ptkovsek M, Dular M, Kompare B, Sirok B, Blazeka Z, Heath E (2013) Removal of pharmaceuticals from wastewater by biological processes, hydrodynamic cavitation and UV treatment. Ultrason Sonochem 20:1104–1112Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • E. Hapeshi
    • 1
    • 2
  • A. Lambrianides
    • 1
    • 2
  • P. Koutsoftas
    • 1
    • 2
  • E. Kastanos
    • 3
  • C. Michael
    • 1
    • 2
  • D. Fatta-Kassinos
    • 1
    • 2
    Email author
  1. 1.Department of Civil and Environmental EngineeringUniversity of CyprusNicosiaCyprus
  2. 2.Nireas International Water Research CenterUniversity of CyprusNicosiaCyprus
  3. 3.Department of Life and Health SciencesUniversity of NicosiaNicosiaCyprus

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