Skip to main content
Log in

UPLC-MS/MS analysis of antibiotics in pharmaceutical effluent in Tunisia: ecotoxicological impact and multi-resistant bacteria dissemination

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The UPLC MS/MS analysis showed the presence of the two antibiotics in the pharmaceutical industry discharges during 3 months; norfloxacin and spiramycin which were quantified with the mean concentrations of 226.7 and 84.2 ng mL−1, respectively. Sixteen resistant isolates were obtained from the pharmaceutical effluent and identified by sequencing. These isolates belong to different genera, namely Citrobacter, Acinetobacter, Pseudomonas, Delftia, Shewanella, and Rheinheimera. The antibiotic resistance phenotypes of these isolates were determined (27 tested antibiotics-discs). All the studied isolates were found resistant to amoxicillin and gentamicin, and 83.33% of isolates were resistant to ciprofloxacin. Multiple antibiotic resistances were revealed against β-lactams, quinolones, and aminoglycosides families. Our overall results suggest that the obtained bacterial isolates may constitute potential candidates for bioremediation and can be useful for biotechnological applications. Genotoxic effects were assessed by a battery of biotests; the pharmaceutical wastewater was genotoxic according to the bacterial Vitotox test and micronuclei test. Genotoxicity was also evaluated by the comet test; the tail DNA damages reached 38 and 22% for concentrated sample (10×) and non-concentrated sample (1×), respectively. However, the histological sections of kidney and liver’s mice treated by pharmaceutical effluent showed normal histology and no visible structural effects or alterations as cytolysis, edema, or ulcerative necrosis were observed. Residual antibiotics can reach water environment through wastewater and provoke dissemination of the antibiotics resistance and induce genotoxic effects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adelowo O, Fagade O, Oke AJ (2008) Prevalence of co-resistance to disinfectants and clinically relevant antibiotics in bacterial isolates from three hospital laboratory wastewaters in southwestern Nigeria. World J Microbiol Biotechnol 25:1993–1997

    Article  CAS  Google Scholar 

  • Albrecht MC, Griffith ME, Murray CK, Chung KK, Horvath EE, Ward JA, Hospenthal DR, Holcomb JB, Wolf SE (2006) Impact of acinetobacter infection on the mortality of burn patients. J Am Coll Surg 203:546–550

    Article  PubMed  Google Scholar 

  • Allen HK, Donato J, Davies J, Wang HH, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8:251–259

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Amos GC, Hawkey PM, Gaze WH, Wellington EM (2014) Waste water effluent contributes to the dissemination of CTX-M-15 in the natural environment. J Antimicrob Chemother 29:1785–1791

    Article  CAS  Google Scholar 

  • Ash RJ, Mauck B, Morgan M (2002) Antibiotic resistance of Gram-negative bacteria in rivers, United States. Emerg Infect Dis 8:713–716

    Article  PubMed  PubMed Central  Google Scholar 

  • Baquero F, Martinez JL, Canton R (2008) Antibiotic and antibiotic resistance in water environments. Curr Opin Biotechnol 19:260–265

    Article  CAS  PubMed  Google Scholar 

  • Baquero F, Tedim AP, Coque TM (2013) Antibiotic resistance shaping multi-level population biology of bacteria. Front Microbiol 4:15. https://doi.org/10.3389/fmicb.2013.00015

    Article  PubMed  PubMed Central  Google Scholar 

  • Beaber JW, Hochhut B, Waldor MK (2004) SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427:72–74

    Article  CAS  PubMed  Google Scholar 

  • Bengtsson-Palme J, Larsson DG (2016) Concentrations of antibiotics predicted to select for resistant bacteria: proposed limits for environmental regulation. Environ Int 86:140–149

    Article  CAS  PubMed  Google Scholar 

  • Birosova L, Mackulak T, Bodak I, Ryba J, Skuback J, Grabic R (2014) Pilot study of seasonal occurrence and distribution of antibiotics and drug resistant bacteria in wastewater treatment plants in Slovakia. Sci Total Environ 490:440–444

    Article  CAS  PubMed  Google Scholar 

  • Bourgeous KN, Darby JL, Tchobanoglous G (2001) Ultrafiltration of wastewater: effects of particles, mode of operation, and backwash effectiveness. Water Res 35:77–90

    Article  CAS  PubMed  Google Scholar 

  • Canton R (2009) Antibiotic resistance genes from the environment: a perspective through newly identified antibiotic resistance mechanisms in the clinical setting. Clin Microbiol Infect 15:20–25

    Article  CAS  PubMed  Google Scholar 

  • Chen B, Yang Y, Liang X, Yu K, Zhang T, Li X (2013) Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments. Environ Sci Technol 47:12753–12760

    Article  CAS  PubMed  Google Scholar 

  • Cleuvers M (2003) Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicol Lett 142:185–194

    Article  CAS  PubMed  Google Scholar 

  • Cleuvers M (2004) Mixture toxicity of the anti-inflammatory drugs diclofenac, ibuprofen, naproxen and acetylsalicylic acid. Ecotoxicol Environ Saf 59:309–315

    Article  CAS  PubMed  Google Scholar 

  • CLSI (2007) Clinical and Laboratory Standards Institute (CLSI), M100-S17. Performance Standards for Antimicrobial Susceptibility Testing, vol 27, (Wayne, PA)

  • Collado N, Rodriguez-Mozaz S, Gros M, Rubirola A, Barcelo D, Comas J, Rodriguez-Roda I, Buttiglieri G (2014) Pharmaceuticals occurrence in a WWTP with significant industrial contribution and its input into the river system. Environ Pollut 185:202–212

    Article  CAS  PubMed  Google Scholar 

  • Commission Decision of 2002/657/EC implementing Council Directive 96/23/EC concerning the performance of analytical methods and the interpretation of results, Off J Eur Commun. 17/08/2002, No. L221/pp 8–36

  • Czekalski N, Berthold T, Caucci S, Egli A, Burgmann H (2012) Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into Lake Geneva, Switzerland. Front Microbiol 3:1–18

    Article  Google Scholar 

  • Daffonchio D, Cherif A, Borin S (2000) Homoduplex and heteroduplex polymorph-isms of the amplified ribosomal 16S–23S internal transcribed spacers describe genetic relationships in the ‘‘Bacillus cereus group’’. Appl Environ Microbiol 66:5460–5468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 107:907–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Costa VM, King CE, Kalan L, Morar M, Sung WW, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD (2011) Antibiotic resistance is ancient. Nature 477:457–461

    Article  PubMed  CAS  Google Scholar 

  • De Castro A, Fenandes G, Franco O (2014) Insights into novel antimicrobial compounds and antibiotic resistance genes from soil metagenomes. Front Microbiol 5:489–498

    Article  PubMed  PubMed Central  Google Scholar 

  • Deschamps E, Vasconcelos O, Lange L, Donnici CL, Da Silva MC, Sales JA, (2012) Management of effluents and waste from pharmaceutical industry in Minas Gerais, Brazil. Brazil J Pharm Sci 48

  • Dhall P, Kumar R, Kumar A (2012) Biodegradation of sewage wastewater using autochthonous bacteria. Sci World J. https://doi.org/10.1100/2012/861903 (ID861903)

    Article  Google Scholar 

  • Dinh QT, Alliot F, Moreau-Guigon E, Eurin J, Chevreuil M, Labadie P (2011) Measurement of trace levels of antibiotics in river water using on-line enrichment and triple quadrupole LC–MS/MS. Talanta 85:1238–1245

    Article  CAS  PubMed  Google Scholar 

  • Dorival-Garcia N, Zafra-Gomez A, Cantarero S, Navalon N, Vilchez JL (2013) Simultaneous determination of 13 quinolones antibiotic derivatives in wastewater samples using solid-phase extraction and ultra performance liquid chromatography–tandem mass spectrometry. Microchem J 106:323–333

    Article  CAS  Google Scholar 

  • Drewnowski J, Makinia J (2014) The role of biodegradable particulate and colloidal organic compounds in biological nutrient removal activated sludge systems. Int J Environ Sci Technol 11:1973–1988

    Article  CAS  Google Scholar 

  • Escher B, Leusch F (2012) Bioanalytical tools in water quality assessment. IWA Publishing, London

    Google Scholar 

  • Ettoumi B, Bouhajja E, Borin S, Daffonchio D, Boudabous A, Cherif A (2010) Gamma-proteobacteria occurrence and microdiversity in Tyrrhenian Sea sediments as revealed by cultivation-dependant and independent approaches. Syst Appl Microbiol 33:222–231

    Article  CAS  PubMed  Google Scholar 

  • Fairburn DW, Olive PL, O’Neill KL (1995) The comet assay: a comprehensive review. Mutat Res 339:37–59

    Article  Google Scholar 

  • Fenech M, Crott JW (2002) Micronuclei, nucleoplasmic bridges and nuclear buds induced in folic acid deficient human lymphocytes-evidence for breakage-fusion-bridge cycles in the cytokinesis-block micronucleus assay. Mutat Res 504:131–136

    Article  CAS  PubMed  Google Scholar 

  • Figueira V, Vaz-Moreira I, Silva M, Manaia CM (2011) Diversity and antibiotic resistance of Aeromonas spp. in drinking and waste water treatment plants. Water Res 45:5599–5611

    Article  CAS  PubMed  Google Scholar 

  • Finley RL, Collignon P, Larsson DG, McEwen SA, Li XZ, Gaze WH, Reid-Smith R, Timinouni M, Graham DW, Topp E (2013) The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis 57:704–710

    Article  PubMed  Google Scholar 

  • Frank-Peterside N, Peekate L, Oriakpono O (2011) Degradation of antibiotics by bacteria and fungi from the aquatic environment. J Toxicol Environ Health Sci 3:275–285

    Google Scholar 

  • Gillings MR (2013) Evolutionary consequences of antibiotic use for the resistome, mobilome and microbial pangenome. Front Microbiol. https://doi.org/10.3389/fmicb.2013.00004

    Article  PubMed  PubMed Central  Google Scholar 

  • Gobel A, McArdell CS, Joss A, Siegrist H, Giger W (2007) Fate of sulfonamides, macrolides, and trimethoprim in different wastewater treatment technologies. Sci Total Environ 372:361–371

    Article  PubMed  CAS  Google Scholar 

  • Goni-Urriza M, Capdepuy Arpin C, Raymond N, Caumette P, Quentin C (2000) Impact of an urban effluent on antibiotic resistant of riverine enterobacteriaceae and Aeromonas sp. Appl Env Microbiol 66:125–132

    Article  CAS  Google Scholar 

  • Gros M, Petrovic M, Ginebreda A, Barcelo D (2010) Removal of pharmaceuticals during wastewater treatment and environmental risk assessment using hazard indexes. Environ Int 36:15–26

    Article  CAS  PubMed  Google Scholar 

  • Gulkowska A, Leung HW, So MK, Taniyasu S, Yamashita N, Yeung LWY, Richardson BJ, Lei AP, Giesy JP, Lam PKS (2008) Removal of antibiotics from wastewater by sewage treatment facilities in Hong Kong and Shenzhen, China. Water Res 42:395–403

    Article  CAS  PubMed  Google Scholar 

  • Gullberg E, Cao S, Berg OG, Ilback C, Sandegren L, Hughes D, Andersson DI (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 1:7–9

    Google Scholar 

  • Hall EK, Neuhauser C, Cotner JB (2008) Toward a mechanistic understanding of how natural bacterial communities respond to changes in temperature in aquatic ecosystems. ISME 2:471–481

    Article  CAS  Google Scholar 

  • Halling-Sorensen B (2000) Inhibition of aerobic growth and nitrification of bacteria in sewage sludge by anti-bacterial agents. Arch Environ Contam Toxicol 40:451–460

    Article  CAS  Google Scholar 

  • Halling-Sorensen B, Holten-Lutzhoft HC, Jorgensen SE (1999) Algal toxicity of antibacterial agents applied in Danish fish farming. Arch Environ Contam Toxicol 36:1–6

    Article  PubMed  Google Scholar 

  • Hartmann A, Alder AC, Koller T, Widmer RM (1998) Identification of fluoroquinolone antibiotics as the main source of umuC genotixicity in native hospital wastewater. Environ Toxicol Chem 17:377–382

    Article  CAS  Google Scholar 

  • Heberer T (2002) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131:5–17

    Article  CAS  PubMed  Google Scholar 

  • Hernando MD, Mezcua M, Fernandez-Alba AR, Barcelo D (2006) Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta 69:334–342

    Article  CAS  PubMed  Google Scholar 

  • Hockenreiner M, Neugebauer H, Elango L (2015) Ex situ bioremediation method for the treatment of groundwater contaminated with PAHs. Int J Environ Sci Technol 12:285–296

    Article  CAS  Google Scholar 

  • Hussain S, Naeem M, Chaudhry MN (2016) Estimation of Residual Antibiotics in Pharmaceutical Effluents and their Fate in Affected Areas. Pol J Environ Stud 25:607–614

    Article  CAS  Google Scholar 

  • Ibegbulam-Njoku PN, Chijioke-Osuji CC, Imo EO (2013) Physicochemical characteristics and biodegradation of pharmaceutical effluent. Int J Sci Eng Res 4:29–38

    Google Scholar 

  • Kaplan E, Ofek M, Jurkevitch E, Cytryn E (2013) Characterization of fluoroquinolone resistance and qnr diversity in Enterobacteriaceae from municipal biosolids. Front Microbiol 1–7

  • Kastenbaum MA, Bowman KO (1970) Tables for determining the statistical significance of mutation frequencies. Mutat Res 9:527–549

    Article  CAS  PubMed  Google Scholar 

  • Kaur R, Dua A (2016) Fish liver and gill cells as cytogenotoxic indicators in assessment of water quality. Environ Sci Pollut Res 23:18892–18900

    Article  CAS  Google Scholar 

  • Kirsch-Volders M, Decordier I, Elhajouji A, Plas G, Aardema MJ, Fenech M (2011) In vitro genotoxicity testing using the micronucleus assay in cell lines, human lymphocytes and 3D human skin models. Mutagenesis 26:177–184

    Article  CAS  PubMed  Google Scholar 

  • Kristiansson E, Fick J, Janzon A, Grabic R, Rutgersson C, Weijdegard B, Soderstrom H, Larsson DG (2011) Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS One 6:e17038. https://doi.org/10.1371/journal.pone.0017038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kudlak B, Wieczerzak M, Yotova G, Tsakovski S, Simeonov V, Namiesnik J (2016) Environmental risk assessment of Polish wastewater treatment plant activity. Chemosphere 160:181–188

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Kungolos AG, Brebbia CA, Samaras CP, Popov V (2006) Environmental toxicology. Southampton, p. 362

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Larsson DG, Pedro C, Paxeus N (2007) Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J Hazard Mater 148:751–755

    Article  CAS  PubMed  Google Scholar 

  • Lateef A (2003) The Microbiology of a Pharmaceutical Effluent and Its Public Health Implications. World J Microb Bio 20:167–171

    Article  Google Scholar 

  • Li D, Qi R, Yang M, Zhang Y, Yu T (2011) Bacterial community characteristics under long-term antibiotic selection pressures. Water Res 45:6063–6073

    Article  CAS  PubMed  Google Scholar 

  • Lindberg RH, Wennberg P, Johansson MI, Tysklind M, Andersson BAV (2005) Screening of Human Antibiotic Substances and Determination of Weekly Mass Flows in Five Sewage Treatment Plants in Sweden. Environ Sci Technol 39:3421–3429

    Article  CAS  PubMed  Google Scholar 

  • Ma D, Hettiarachchi G, Nguyen D, Zhang B, Wittenberg JB, Zavalij PY, Briken V, Isaacs L (2012) Acyclic cucurbituril molecular containers enhance the solubility and bioactivity of poorly soluble pharmaceuticals. Nat Chem J 4:503–510

    Article  CAS  Google Scholar 

  • Maranho LA, Baena-Nogueras RM, Lara-Martín PA, DelValls TA, Martin-Diaz ML (2014) Bioavailability, oxidative stress, neurotoxicity and genotoxicity of pharmaceuticals bound to marine sediments. The use of the polychaete Hediste diversicolor as bioindicator species. Environ Res 134:353–365

    Article  CAS  PubMed  Google Scholar 

  • Marti E, Variatza E, Balcazar JL (2014) The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol 22:36–41

    Article  CAS  PubMed  Google Scholar 

  • Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902

    Article  CAS  PubMed  Google Scholar 

  • Mater N, Geret F, Castillo L, Faucet-Marquis V, Albasi C, Pfohl-Leszkowicz A (2014) In vitro tests aiding ecological risk assessment of ciprofloxacin, tamoxifen and cyclophosphamide in range of concentrations released in hospital wastewater and surface water. Environ Int 63:191–200

    Article  CAS  PubMed  Google Scholar 

  • Mathur N, Bhatnagar P, Mohan K, Bakre P, Nagar P, Bijarnia M (2007) Mutagenicity evaluation of industrial sludge from common effluent treatment plant. Chemosphere 67:1229–1235

    Article  CAS  PubMed  Google Scholar 

  • Miao XS, Koenig BG, Metcalfe CD (2002) Analysis of acidic drugs in the effluents of sewage treatment plants using liquid chromatography–electrospray ionization tandem mass spectrometry. J Chromatogr A 952:139–147

    Article  CAS  PubMed  Google Scholar 

  • Musolff A, Leschik S, Möder M, Strauch G, Reinstorf F, Schirmer M (2009) Temporal and spatial patterns of micropollutants in urban receiving waters. Environ Pollut 157:3069–3077

    Article  CAS  PubMed  Google Scholar 

  • Novo A, Manaia CM (2010) Factors influencing antibiotic resistance burden in municipal wastewater treatment plants. Appl Microbiol Biotechnol 87:1157–1166

    Article  CAS  PubMed  Google Scholar 

  • Novo A, Andre S, Viana P, Nunes OC, Manaia CM (2013) Antibiotic resistance, antimicrobial residues and bacterial community composition in urban wastewater. Water Res 47:1875–1887

    Article  CAS  PubMed  Google Scholar 

  • Oh HS, Kum KA, Kim EC, Lee HJ, Choe KW, Oh MD (2008) Outbreak of Shewanella algaeand Shewanella putrefaciens infections caused by a shared measuring cup in a general surgery unit in Korea. Infect Control Hosp Epidemiol 29:742–748

    Article  PubMed  Google Scholar 

  • Ohara CM, Brenner FW, Miller JM (2000) Classification, identification, and clinical significance of proteus, providencia, and morganella. Clin Microbiol Rev 13:534–546

    Article  CAS  Google Scholar 

  • Oren A (2014) The prokaryotes, the family Rhodocyclaceae. Springer, Berlin, pp 975–998

    Book  Google Scholar 

  • Parolini M, Magni M, Castiglioni S, Binelli A (2016) Genotoxic effects induced by the exposure to an environmental mixture of illicit drugs to the zebra mussel. Ecotoxicol Environ Saf 132:26–30

    Article  CAS  PubMed  Google Scholar 

  • Pei R, Kim SC, Carlson KH, Pruden A (2006) Effect of River Landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res 40:2427–2435

    Article  CAS  PubMed  Google Scholar 

  • Pomati F, Orlandi C, Clerici M, Luciani F, Zuccato E (2008) Effects and interactions in an environmentally relevant mixture of pharmaceuticals. Toxicol Sci. 102:129–137

    Article  CAS  PubMed  Google Scholar 

  • Pruden A, Larsson DG, Amézquita A, Collignon P, Brandt KK, Graham DW, Lazorchak JM, Suzuki S, Silley P, Snape JR, Topp E, Zhang T, Zhu YG (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect 121:878–885

    Article  PubMed  PubMed Central  Google Scholar 

  • Qin JJ, Oo MH, Wai MN, Kekre KA (2005) TOC removal in reclamation of municipal wastewater by RO. SepPurif Technol 46:125–128

    Article  CAS  Google Scholar 

  • Rao V, Dhar RL, Subrahmanyam K (2001) Assessment of contaminant migration in groundwater from an industrial developpment area, Medak district, Andhra Pradesh. Water Air Soil Pollut 12:369–389

    Google Scholar 

  • Sarmah AK, Meyer MT, Boxall AB (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759

    Article  CAS  PubMed  Google Scholar 

  • Schluter A, Szczepanowski R, Kurz N, Schneiker S, Krahn I, Puhler A (2007) Erythromycin resistance-conferring plasmid pRSB105, isolated from a sewage treatment plant, harbors a new macrolide resistance determinant, an integron-containing Tn402-like element, and a large region of unknown function. Appl Environ Microbiol 73:1952–1960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharif A, Ashraf M, Anjum AA, Javeed A, Altaf I, Akhtar MF, Abbas M, Akhtar B, Saleem A (2016) Pharmaceutical wastewater being composite mixture of environmental pollutants may be associated with mutagenicity and genotoxicity. Environ Sci Pollut Res Int 23:2813–2820

    Article  CAS  PubMed  Google Scholar 

  • Sigee DC (2005) Freshwater microbiology: biodiversity and dynamic interactions of microorganisms in the aquatic environment. Wiley, West Sussex

    Google Scholar 

  • Singleton DR, Dickey AN, Scholl EH, Wright FA, Aitken MD (2015) Complete genome sequence of a novel bacterium within the family Rhodocyclaceae that degrades polycyclic aromatic hydrocarbons. Genome Announc. https://doi.org/10.1128/genomeA00251-15

    Article  PubMed  PubMed Central  Google Scholar 

  • Solomons IA (1978) Antibiotics in animal feeds Human and animal safety issues. J Ani Sci 46:1360–1368

    Article  CAS  Google Scholar 

  • Sturm RN (1973) Biodegradability of nonionic surfactants screening test for predicting rate and ultimate biodegradation. J Am Oil Chem Soc 50:159–167

    Article  CAS  Google Scholar 

  • Tahrani L, Soufi L, Mehri I, Najjari A, Hassan A, Van Loco J, Reyns T, Cherif A, Ben Mansour H (2015) Isolation and characterization of antibiotic-resistant bacteria frompharmaceutical industrial wastewaters. Microb Pathog 89:54–61

    Article  CAS  PubMed  Google Scholar 

  • Tahrani L, Van Loco J, Ben Mansour H, Reyns T (2016) Occurrence of antibiotics in pharmaceutical industrial wastewater, wastewater treatment plant and sea waters in Tunisia. J Water Health 14:208–213

    Article  PubMed  Google Scholar 

  • Takanashi H, Kishida M, Nakajima T, Ohki A, Akiba M, Aizawa T (2009) Surveying the mutagenicity of tap water to elicit the effects of purification processes on Japanese tap water. Chemosphere 77:434–439

    Article  CAS  PubMed  Google Scholar 

  • Tennstedt T, Szczepanowski R, Krahn I, Puhler A, Schluter A (2005) Sequence of the 68,869 bp IncP-1alpha plasmid pTB11 from a waste-water treatment plant reveals a highly conserved backbone, a Tn402-like integron and other transposable elements. Plasmid 53:218–238

    Article  CAS  PubMed  Google Scholar 

  • Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221

    Article  CAS  PubMed  Google Scholar 

  • Varela AR, Andre S, Nunes O, Manaia C (2014) Insights into the relationship between antimicrobial residues and bacterial populations in a hospital-urban wastewater treatment plant system. Water Res 54:327–336

    Article  CAS  PubMed  Google Scholar 

  • Verschaeve L (2002) Genotoxicity studies in groundwater, surface waters, and contaminated soil. Sci World J 2:1247–1253

    Article  CAS  Google Scholar 

  • Verschaeve L, Van Gompel J, Thilemans L, Regniers L, Vanparys P, Van der Lelie D (1999) VITOTOX® bacterial genotoxicity and toxicity test for the rapid screening of chemicals. Environ Mol Mutagen 33:240–248

    Article  CAS  PubMed  Google Scholar 

  • Verschaeve L, Mertens B, Ndhlala AR, Anthonissen R, Gorissen B, Van Staden BJ (2012) Extracts from Hypoxis Species and a Commercially Available Hypoxis Preparation. Phytother Res 27:350–356

    Article  PubMed  Google Scholar 

  • Watkinson AJ, Murbyc EJ, Costanzo SD (2007) Removal of antibiotics in conventional and advanced wastewater treatment: implications for environmental discharge and wastewater recycling. Water Res 41:4164–4176

    Article  CAS  PubMed  Google Scholar 

  • Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP (2013) The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect Dis 13:155–165

    Article  CAS  PubMed  Google Scholar 

  • Wollenberger L, Halling-Soerensen B, Kusk KO (2000) Acute and chronic toxicity of veterinary antibiotics to Daphnia magna. Chemosphere 70:723–730

    Article  Google Scholar 

  • Yan C, Dinh QT, Chevreuil M, Garnier J, Roose-Amsaleg C, Labadie P, Laverman AM (2013) The effect of environmental and therapeutic concentrations of antibiotics on nitrate reduction rates in river sediment. Water Res 47:3654–3662

    Article  CAS  PubMed  Google Scholar 

  • Zegura B, Heath E, Cernosa A, Filipic M (2009) Combination of in vitro bioassays for the determination of cytotoxic and genotoxic potential of wastewater, surface water and drinking water samples. Chemosphere 75:1453–1460

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zhang T, Fang HP (2009) Antibiotic resistance genes in water environment. Appl Micobiol Biotechnol 82:397–414

    Article  CAS  Google Scholar 

  • Zhang S, Yang G, Hou S, Wang Y (2011) Abundance and diversity of glacial bacteria on the Tibetan Plateau with environment. Geomicrobiol J 27:649–655

    Article  Google Scholar 

  • Zhou JL, Maskaoui K, Lufadeju A (2012) Optimization of antibiotic analysis in water by solid-phase extraction and high performance liquid chromatography-mass spectrometry/mass spectrometry. Anal ChimActa 731:32–39

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hedi Ben Mansour.

Additional information

Communicated by Djamel DRIDER.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tahrani, L., Mehri, I., Reyns, T. et al. UPLC-MS/MS analysis of antibiotics in pharmaceutical effluent in Tunisia: ecotoxicological impact and multi-resistant bacteria dissemination. Arch Microbiol 200, 553–565 (2018). https://doi.org/10.1007/s00203-017-1467-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-017-1467-x

Keywords

Navigation