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Status of pathogens, antibiotic resistance genes and antibiotic residues in wastewater treatment systems

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Abstract

Pathogens are becoming nearly untreatable due to the rise in gaining new resistance against standard antibiotics. Coexistence of microbial pathogens, antibiotics and antibiotic resistant genes (ARGs) in wastewater treatment plants (WWTP) provide favourable conditions for the development of new antibiotic resistant bacteria (ARB); facilitate horizontal gene transfer among pathogens and may also serve as a hotspot for the spread of ARB and genes into the environment. In this study, the current status of wastewater treatment systems in the removal of pathogens, ARGs, and antibiotic residues are discussed. WWTP are efficient in removing pathogens and antibiotic residues to a greater extend during secondary and tertiary treatment processes. Recent studies, however, have shown high variations in the presence of pathogens including ARB as well as antibiotic resistance genes (ARG) in the final effluent. Prolonged sludge retention time (SRT) and hydraulic retention time (HRT) during secondary treatment will facilitate antibiotic removal by adsorption and biodegradation. However, the above conditions can also lead to the enhancement of antibiotic resistance process in microbes. Therefore, optimum conditions for the operation of conventional WWTP for the efficient removal of antibiotics are yet to be established. The removal of antibiotic residues can be accelerated by combining conventional activated sludge (CAS) process with an additional treatment technology involving dosing with ozone. The advanced biological treatment method using membrane bioreactors (MBR) in combination with coagulation reportedly has the best ARG removal efficiency, and removes both ARB and extracellular ARGs. While studies have predicted the fate for ARGs in wastewater treatment plants, the mechanisms of ARGs acquisition remains to be conclusively established. Thus, strategies to investigate the underlying mechanism of acquisition of ARGs within the WWTP are also provided in this review.

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References

  • Abd H, Saeed A, Weintraub A, Nair GB, Sandström G (2007) Vibrio cholerae O1 strains are facultative intracellular bacteria, able to survive and multiply symbiotically inside the aquatic free-living amoeba Acanthamoeba castellanii. FEMS Microbiol Ecol 60:33

    Article  CAS  Google Scholar 

  • Al Mamun AAM et al (2012) Identity and function of a large gene network underlying mutagenic repair of DNA breaks. Science 338:1344–1348. doi:10.1126/science.1226683

    Article  CAS  Google Scholar 

  • Al-Bahry SN, Paulson J, Al-Musharaf S (2015) Survival and growth of bacteria in treated wastewater and water distribution systems and their implication in human health: A review. IAJAA 4

  • Al-Jassim N, Ansari MI, Harb M, Hong P-Y (2015) Removal of bacterial contaminants and antibiotic resistance genes by conventional wastewater treatment processes in Saudi Arabia: is the treated wastewater safe to reuse for agricultural irrigation? Water Res 73:277–290

    Article  CAS  Google Scholar 

  • Alouache S, Estepa V, Messai Y, Ruiz E, Torres C, Bakour R (2014) Characterization of ESBLs and associated quinolone resistance in Escherichia coli and Klebsiella pneumoniae isolates from an urban wastewater treatment plant in Algeria. Microb Drug Resist 20:30–38. doi:10.1089/mdr.2012.0264

    Article  CAS  Google Scholar 

  • Amador PP, Fernandes RM, Prudencio MC, Barreto MP, Duarte IM (2015) Antibiotic resistance in wastewater: occurrence and fate of Enterobacteriaceae producers of class A and class C beta-lactamases. J Environ Sci Health A Tox Hazard Subst Environ Eng 50:26–39. doi:10.1080/10934529.2015.964602

    Article  CAS  Google Scholar 

  • Amin MT, Alazba AA, Manzoor U (2014) A review of removal of pollutants from water/wastewater using different types of nanomaterials. Adv Mater Sci Eng 2014:24. doi:10.1155/2014/825910

    Article  CAS  Google Scholar 

  • Awuah E (2006) Pathogen removal mechanisms in waste stabilisation ponds. Ph.D. Thesis, Wageningen University/UNESCO-IHE Institute for Water Education,Wageningen, The Netherlands

  • Aziz MA, Surveillance WIGPoA-tDR (2004) Anti-tuberculosis Drug Resistance in the World: Third Global Report: the WHO/IUATLD global project on anti-tuberculosis drug resistance surveillance, 3 1999–2002. World Health Organization

  • Badela AU (2014) Prevalence and pathogenicity of vibrios in treated final effluents of selected wastewater treatment plants in the amathole district municipality of Eastern Cape Province of South Africa. University of Fort Hare Masters Thesis

  • Bahl MI, Hansen LH, Goesmann A, Sørensen SJ (2007) The multiple antibiotic resistance IncP-1 plasmid pKJK5 isolated from a soil environment is phylogenetically divergent from members of the previously established α, β and δ sub-groups. Plasmid 58:31–43

    Article  CAS  Google Scholar 

  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182

    Article  CAS  Google Scholar 

  • Balcázar JL, Subirats J, Borrego CM (2015) The role of biofilms as environmental reservoirs of antibiotic resistance. Front Microbiol. doi:10.3389/fmicb.2015.01216

    Google Scholar 

  • Batt AL, Bruce IB, Aga DS (2006) Evaluating the vulnerability of surface waters to antibiotic contamination from varying wastewater treatment plant discharges. Environ Pollut 142:295–302. doi:10.1016/j.envpol.2005.10.010

    Article  CAS  Google Scholar 

  • Batt AL, Kim S, Aga DS (2007) Comparison of the occurrence of antibiotics in four full-scale wastewater treatment plants with varying designs and operations. Chemosphere 68:428–435

    Article  CAS  Google Scholar 

  • Bengtsson-Palme J et al (2016) Elucidating selection processes for antibiotic resistance in sewage treatment plants using metagenomics. Sci Total Environ 572:697–712

    Article  CAS  Google Scholar 

  • Berendonk TU et al (2015) Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol 13:310–317

    Article  CAS  Google Scholar 

  • Berjeaud J-M et al. (2016) Legionella pneumophila: The paradox of a highly sensitive opportunistic waterborne pathogen able to persist in the environment. Front Microbiol 7

  • Berkner S, Konradi S, Schönfeld J (2014) Antibiotic resistance and the environment—there and back again. EMBO Rep 15:740–744. doi:10.15252/embr.201438978

    Article  CAS  Google Scholar 

  • Blaak H, Lynch G, Italiaander R, Hamidjaja RA, Schets FM, de Roda Husman AM (2015) Multidrug-resistant and extended spectrum beta-lactamase-producing Escherichia coli in Dutch surface water and wastewater. PLoS One 10:e0127752. doi:10.1371/journal.pone.0127752

    Article  CAS  Google Scholar 

  • Börjesson S (2009) Antibiotic resistance in Wastewater: Methicillin-resistant Staphylococcus aureus (MRSA) and antibiotic resistance genes. Doctoral dissertation. University Electronic Press, Linköping

    Google Scholar 

  • Boucher Y, Labbate M, Koenig JE, Stokes HW (2007) Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol 15:301–309

    Article  CAS  Google Scholar 

  • Bouki C, Venieri D, Diamadopoulos E (2013) Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: a review Ecotoxicol. Environ Safe 91:1–9

    Article  CAS  Google Scholar 

  • Bryce A, Hay AD, Lane IF, Thornton HV, Wootton M, Costelloe C (2016) Global prevalence of antibiotic resistance in paediatric urinary tract infections caused by Escherichia coli and association with routine use of antibiotics in primary care: systematic review and meta-analysis. BMJ 352:i939

    Article  CAS  Google Scholar 

  • Burkhardt Iii W, Calci KR, Watkins WD, Rippey SR, Chirtel SJ (2000) Inactivation of indicator microorganisms in estuarine waters. Water Res 34:2207–2214. doi:10.1016/S0043-1354(99)00399-1

    Article  Google Scholar 

  • Butkovskyi A, Leal LH, Rijnaarts H, Zeeman G (2015) Fate of pharmaceuticals in full-scale source separated sanitation system. Water Res 85:384–392

    Article  CAS  Google Scholar 

  • Byarugaba DK, Kisame R, Olet S (2011) Multi-drug resistance in commensal bacteria of food of animal origin in Uganda. Afr J Microbiol Res 5:1539–1548

    Article  Google Scholar 

  • Cai L, Zhang T (2013) Detecting human bacterial pathogens in wastewater treatment plants by a high-throughput shotgun sequencing technique. Environ Sci Technol 47:5433–5441. doi:10.1021/es400275r

    Article  CAS  Google Scholar 

  • Cao B, Gao B, Liu X, Wang M, Yang Z, Yue Q (2011) The impact of pH on floc structure characteristic of polyferric chloride in a low DOC and high alkalinity surface water treatment. Water Res 45:6181–6188

    Article  CAS  Google Scholar 

  • Castiglioni S, Bagnati R, Fanelli R, Pomati F, Calamari D, Zuccato E (2006) Removal of pharmaceuticals in sewage treatment plants in Italy. Environ Sci Technol 40:357–363

    Article  CAS  Google Scholar 

  • CDDEP Center for Disease Dynamics, Economics and Policy (2015) State of the World’s Antibiotics, 2015. CDDEP, Washington

    Google Scholar 

  • Chae SR et al (2014) Advanced wastewater treatment using mbrs: Nutrient removal and disinfection. In: Hai FI, Yamamoto K, Lee C-H (eds) membrane biological reactors: Theory, modeling, design, management and applications to wastewater reuse. IWA publishers, London, pp 137–163

    Google Scholar 

  • Chambers HF, DeLeo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7:629–641

    Article  CAS  Google Scholar 

  • Chan K-G (2016) Whole-genome sequencing in the prediction of antimicrobial resistance. Expert Rev Anti Infect Ther 14:617–619. doi:10.1080/14787210.2016.1193005

    Article  CAS  Google Scholar 

  • Charlotte (2015) Wastewater treatment may be creating new antibiotics. ScienceDaily. Retrieved October 28, 2016 from www.sciencedaily.com/releases/2015/05/150528123858.htm

  • Chen H, Zhang M (2013) Effects of advanced treatment systems on the removal of antibiotic resistance genes in wastewater treatment plants from Hangzhou. China Environ Sci Technol 47:8157–8163

    CAS  Google Scholar 

  • Chen J et al (2016) Removal of antibiotics and antibiotic resistance genes from domestic sewage by constructed wetlands: Effect of flow configuration and plant species. Sci Total Environt 571:974–982. doi:10.1016/j.scitotenv.2016.07.085

    Article  CAS  Google Scholar 

  • Chisholm SA, Owen RJ, Teare EL, Saverymuttu S (2001) PCR-based diagnosis of Helicobacter pylori infection and real-time determination of clarithromycin resistance directly from human gastric biopsy samples. J Clin Microbiol 39:1217–1220

    Article  CAS  Google Scholar 

  • Christgen B, Yang Y, Ahammad SZ, Li B, Rodriquez DC, Zhang T, Graham DW (2015) Metagenomics shows that low-energy anaerobic—eerobic treatment reactors reduce antibiotic resistance gene levels from domestic wastewater. Environ Sci Technol 49:2577–2584. doi:10.1021/es505521w

    Article  CAS  Google Scholar 

  • Chubar N, Behrends T, Van Cappellen P (2008) Biosorption of metals (Cu 2 +, Zn 2 +) and anions (F−, H 2 PO 4−) by viable and autoclaved cells of the gram-negative bacterium Shewanella putrefaciens. Colloids Surfs B 65:126–133

    Article  CAS  Google Scholar 

  • Chunhui Z, Liangliang W, Xiangyu G, Xudan H (2016) Antibiotics in WWTP discharge into the Chaobai River, Beijing. Arch Environ Prot 42:48–57

    Google Scholar 

  • Churchyard G et al (2014) Tuberculosis control in South Africa: successes, challenges and recommendations. S Afr Med J 104:234–248

    Google Scholar 

  • Cirz RT, Romesberg FE (2007) Controlling Mutation: intervening in evolution as a therapeutic strategy. Crit Rev Biochem Mol Biol 42:341–354

    Article  CAS  Google Scholar 

  • Cirz RT, O’Neill BM, Hammond JA, Head SR, Romesberg FE (2006) Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J Bacteriol 188:7101–7110

    Article  CAS  Google Scholar 

  • Cirz RT, Jones MB, Gingles NA, Minogue TD, Jarrahi B, Peterson SN, Romesberg FE (2007) Complete and SOS-mediated response of Staphylococcus aureus to the Antibiotic Ciprofloxacin. J Bacteriol 189:531–539. doi:10.1128/jb.01464-06

    Article  CAS  Google Scholar 

  • Clara M, Kreuzinger N, Strenn B, Gans O, Kroiss H (2005) The solids retention time—a suitable design parameter to evaluate the capacity of wastewater treatment plants to remove micropollutants. Water Res 39:97–106

    Article  CAS  Google Scholar 

  • Cohen Nadia R, Lobritz Michael A, Collins James J (2013) Microbial persistence and the road to drug resistance. Cell Host Microbe 13:632–642. doi:10.1016/j.chom.2013.05.009

    Article  CAS  Google Scholar 

  • Cui Q, Fang T, Huang Y, Dong P, Wang H (2017) Evaluation of bacterial pathogen diversity, abundance and health risks in urban recreational water by amplicon next-generation sequencing and quantitative PCR. J Environ Sci 57:137–149

    Article  Google Scholar 

  • Cydzik-Kwiatkowska A, Zielińska M (2016) Bacterial communities in full-scale wastewater treatment systems. World J Microbiol Biotechnol 32:66. doi:10.1007/s11274-016-2012-9

    Article  CAS  Google Scholar 

  • Czekalski N, Berthold T, Caucci S, Egli A, Buergmann H (2012) Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into Lake Geneva. Switzerland Front Microbiol. doi:10.3389/fmicb.2012.00106

    Google Scholar 

  • Danielle Petterson (2016) SA’s waste water treatment works in bad shape. In Effluent, News, Water. Accesssed 03/04/2017 http://www.infrastructurene.ws/2016/05/10/sas-waste-water-treatment-works-in-bad-shape/.

  • Department of Health (2015) Health on antibiotics resistance South Africa

  • Deshmukh RA, Joshi K, Bhand S, Roy U (2016) Recent developments in detection and enumeration of waterborne bacteria: a retrospective minireview. Microbiologyopen 5:901–922

    Article  Google Scholar 

  • Dodd MC (2012) Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. J Environ Monit 14:1754–1771

    Article  CAS  Google Scholar 

  • Dolejska M et al (2012) Dissemination of IncFIIK-type plasmids in multiresistant CTX-M-15-producing Enterobacteriaceae isolates from children in hospital paediatric oncology wards. Int J Antimicrob Agents 40:510–515. doi:10.1016/j.ijantimicag.2012.07.016

    Article  CAS  Google Scholar 

  • Elmund GK, Morrison SM, Grant DW, Nevins SM (1971) Role of excreted chlortetracycline in modifying the decomposition process in feedlot waste. Bull Environ Contam Toxicol 6:129–132

    Article  CAS  Google Scholar 

  • Feinman S, Matheson J (1978) Draft environmental impact statement: subtherapeutic antibacterial agents in animal feeds. Food and Drug Administration Department of Health, Education and Welfare Report. Washington, D.C.: Food and Drug Administration;. p. 372

  • Fekadu S, Merid Y, Beyene H, Teshome W, Gebre-Selassie S (2015) Assessment of antibiotic- and disinfectant-resistant bacteria in hospital wastewater, south Ethiopia: a cross-sectional study. J Infect Dev Ctries 9:149–156. doi:10.3855/jidc.4808

    Article  Google Scholar 

  • Figueroa RA, Leonard A, MacKay AA (2004) Modeling tetracycline antibiotic sorption to clays. Environ Sci Technol 38:476–483

    Article  CAS  Google Scholar 

  • Fokazi S (2015) SA antibiotic use up 60% in 10 years. Daily news, Lifestyle. 18 September 2015

  • Francy DS et al (2012) Comparative effectiveness of membrane bioreactors, conventional secondary treatment, and chlorine and UV disinfection to remove microorganisms from municipal wastewaters. Water Res 46:4164–4178

    Article  CAS  Google Scholar 

  • Furuya EY, Lowy FD (2006) Antimicrobial-resistant bacteria in the community setting. Nat Rev Microbiol 4:36–45

    Article  CAS  Google Scholar 

  • Galler H et al (2014) KPC-2 and OXA-48 carbapenemase-harbouring Enterobacteriaceae detected in an Austrian wastewater treatment plant. Clin Microbiol Infect 20:O132–O134

    Article  CAS  Google Scholar 

  • Gao B, Liu B, Chen T, Yue Q (2011) Effect of aging period on the characteristics and coagulation behavior of polyferric chloride and polyferric chloride–polyamine composite coagulant for synthetic dying wastewater treatment. J Hazard Mater 187:413–420

    Article  CAS  Google Scholar 

  • Gao P, Munir M, Xagoraraki I (2012) Correlation of tetracycline and sulfonamide antibiotics with. corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant. Sci Total Environ 421:173–183

    Article  CAS  Google Scholar 

  • Gatica J, Kaplan E, Cytryn E (2016) Antibiotic resistance elements in wastewater treatment plants: scope and potential impacts. In: Fatta-Kassinos D, Dionysiou DD, Kümmerer K (eds) Wastewater reuse and Current Challenges. Springer, Cham. doi:10.1007/698_2015_361

    Google Scholar 

  • Gelbrand H et al (2015) The state of the world’s antibiotics 2015. Wound Healing Southern Africa 8:30–34

    Google Scholar 

  • Gillespie SH (2002) Evolution of drug resistance in Mycobacterium tuberculosis: clinical and molecular perspective. Antimicrob Agents Chemother 46:267–274. doi:10.1128/aac.46.2.267-274.2002

    Article  CAS  Google Scholar 

  • Gillings MR (2014) Integrons: past, Present, and Future. Microbiol Mol Biol Rev 78:257–277. doi:10.1128/mmbr.00056-13

    Article  CAS  Google Scholar 

  • Göbel A, Thomsen A, McArdell CS, Joss A, Giger W (2005) Occurrence and sorption behavior of sulfonamides, macrolides, and trimethoprim in activated sludge treatment. Environ Sci Technol 39:3981–3989. doi:10.1021/es048550a

    Article  CAS  Google Scholar 

  • Golkar Z, Bagasra O, Pace DG (2014) Bacteriophage therapy: a potential solution for the antibiotic resistance crisis. J Infect Dev Ctries 8:129–136. doi:10.3855/jidc.3573

    Article  Google Scholar 

  • Goñi P, Fernández MT, Rubio E (2014) Identifying endosymbiont bacteria associated with free-living amoebae. Environ Microbiol 16:339–349

    Article  Google Scholar 

  • Gopo Q (2013) Regulation of wastewater treatment plants in the Ba-Phalaborwa Municipality. North-West University, Evanston

    Google Scholar 

  • Gould IM, Bal AM (2013) New antibiotic agents in the pipeline and how they can help overcome microbial resistance. Virulence 4:185–191

    Article  Google Scholar 

  • Greub G, Raoult D (2004) Microorganisms resistant to free-living Amoebae. Clin Microbiol Rev 17:413–433. doi:10.1128/cmr.17.2.413-433.2004

    Article  Google Scholar 

  • Hadjoudja S, Deluchat V, Baudu M (2010) Cell surface characterisation of Microcystis aeruginosa and Chlorella vulgaris . J Colloid Interface Sci 342:293–299

    Article  CAS  Google Scholar 

  • Hai FI, Riley T, Shawkat S, Magram SF, Yamamoto K (2014) Removal of pathogens by membrane bioreactors: a review of the mechanisms, influencing factors and reduction in chemical disinfectant dosing. Water 6:3603–3630

    Article  Google Scholar 

  • Harb M, Hong P-Y (2017) Molecular-based detection of potentially pathogenic bacteria in membrane bioreactor (MBR) systems treating municipal wastewater: a case study. Environ Sci Pollut Res Int 24:5370–5380. doi:10.1007/s11356-016-8211-y

    Article  CAS  Google Scholar 

  • Hendricks R, Pool EJ (2012) The effectiveness of sewage treatment processes to remove faecal pathogens and antibiotic residues. J Environ Sci Health A Tox Hazard Subst Environ Eng Part A, Toxic/Hazardous Subst Environ Eng 47:289–297

    Article  CAS  Google Scholar 

  • Heuer H et al (2012) IncP-1ε Plasmids are Important Vectors of Antibiotic Resistance Genes in Agricultural Systems: diversification driven by class 1 integron Gene Cassettes front. Microbiol. doi:10.3389/fmicb.2012.00002

    Google Scholar 

  • Hill KE, Weightman AJ, Fry JC (1992) Isolation and screening of plasmids from the epilithon which mobilize recombinant plasmid pD10. Appl Environ Microbiol 58:1292–1300

    CAS  Google Scholar 

  • Hrenovic J, Goic-Barisic I, Kazazic S, Kovacic A, Ganjto M, Tonkic M (2016) Carbapenem-resistant isolates of Acinetobacter baumannii in a municipal wastewater treatment plant, Croatia, 2014. Eurosurveillance 21. doi:10.2807/1560-7917.es.2016.21.15.30195

  • Huang J-J, Hu H-Y, Tang F, Li Y, Lu S-Q, Lu Y (2011) Inactivation and reactivation of antibiotic-resistant bacteria by chlorination in secondary effluents of a municipal wastewater treatment plant. Water Res 45:2775–2781

    Article  CAS  Google Scholar 

  • Huang K, Tang J, Zhang X-X, Xu K, Ren H (2014) A comprehensive insight into tetracycline resistant bacteria and antibiotic resistance genes in activated sludge using next-generation sequencing Int. J Mol Sci 15:10083–10100

    Article  CAS  Google Scholar 

  • Huber MM, Korhonen S, Ternes TA, von Gunten U (2005a) Oxidation of pharmaceuticals during water treatment with chlorine dioxide. Water Res 39:3607–3617

    Article  CAS  Google Scholar 

  • Huber MM et al (2005b) Oxidation of pharmaceuticals during ozonation of municipal wastewater effluents: a pilot study. Environ Sci Technol 39:4290–4299

    Article  CAS  Google Scholar 

  • Ikehata K, Gamal El-Din M, Snyder SA (2008) Ozonation and advanced oxidation treatment of emerging organic pollutants in water and wastewater. Ozone Sci Eng 30:21–26

    Article  CAS  Google Scholar 

  • Iweriebor BC, Obi LC, Okoh AI (2015) Virulence and antimicrobial resistance factors of Enterococcus spp. isolated from fecal samples from piggery farms in Eastern Cape, South Africa. BMC Microbiol 15:1

    Article  Google Scholar 

  • Jiang M, Wang L, Ji R (2010) Biotic and abiotic degradation of four cephalosporin antibiotics in a lake surface water and sediment. Chemosphere 80:1399–1405

    Article  CAS  Google Scholar 

  • Jjemba PK, Johnson W, Bukhari Z, LeChevallier MW (2015) Occurrence and control of Legionella in recycled water systems. Pathogens 4:470–502

    Article  Google Scholar 

  • Ju F, Li B, Ma L, Wang Y, Huang D, Zhang T (2016) Antibiotic resistance genes and human bacterial pathogens: co-occurrence, removal, and enrichment in municipal sewage sludge digesters. Water Res 91:1–10. doi:10.1016/j.watres.2015.11.071

    Article  CAS  Google Scholar 

  • Kanabus A (2016) “Information about Tuberculosis”, GHE, 2016, www.tbfacts.org

  • Karimi Fatemeh, Samarghandi Mohammad Reza, Shokohi Reza, Arabestani Mohammad Reza (2016) Prevalence and removal efficiency of Enterococcal Species and vancomycin-resistant Enterococci of a hospital wastewater treatment plant. Avicenna J Environ Health Eng 3(2):e8623

    Google Scholar 

  • Kim S, Eichhorn P, Jensen JN, Weber AS, Aga DS (2005) Removal of antibiotics in wastewater: effect of hydraulic and solid retention times on the fate of tetracycline in the activated sludge process. Environ Sci Technol 39:5816–5823

    Article  CAS  Google Scholar 

  • Klümper U, Dechesne A, Smets BF (2014a) Protocol for evaluating the permissiveness of bacterial communities toward conjugal plasmids by quantification and isolation of transconjugants. In. Humana Press, Totowa, pp 1–14. doi:10.1007/8623_2014_36

  • Klümper U, Droumpali A, Dechesne A, Smets BF (2014b) Novel assay to measure the plasmid mobilizing potential of mixed microbial communities. Front Microbiol. doi:10.3389/fmicb.2014.00730

    Google Scholar 

  • Kraume M, Drews A (2010) Membrane bioreactors in waste water treatment–status and trends. Chem Eng Technol 33:1251–1259

    Article  CAS  Google Scholar 

  • Kumaraswamy R, Amha YM, Anwar MZ, Henschel A, Rodriguez J, Ahmad F (2014) Molecular analysis for screening human bacterial pathogens in municipal wastewater treatment and reuse. Environ Sci Technol 48:11610–11619. doi:10.1021/es502546t

    Article  CAS  Google Scholar 

  • Kümmerer K, Al-Ahmad A (1997) Biodegradability of the anti-tumour agents 5-Fluorouracil cytarabine, and gemcitabine: impact of the chemical structure and synergistic toxicity with hospital effluent. Acta Hydroch Hydrob 25:166–172

    Article  Google Scholar 

  • Laxminarayan R, Chaudhury RR (2016) Antibiotic resistance in India: drivers and opportunities for action. PLoS Medicine 13:e1001974. doi:10.1371/journal.pmed.1001974

    Article  Google Scholar 

  • Lei G, Ma J, Guan X, Song A, Cui Y (2009) Effect of basicity on coagulation performance of polyferric chloride applied in eutrophicated raw water. Desalination 247:518–529

    Article  CAS  Google Scholar 

  • Len Y, Wen-Shi C, Mong-Na LH (2000) Natural disinfection of wastewater in marine outfields. Water Res 34:743–750

    Article  Google Scholar 

  • Li B, Zhang T (2010) Biodegradation and adsorption of antibiotics in the activated sludge process. Environ Sci Technol 44:3468–3473. doi:10.1021/es903490h

    Article  CAS  Google Scholar 

  • Li W, Shi Y, Gao L, Liu J, Cai Y (2013) Occurrence and removal of antibiotics in a municipal wastewater reclamation plant in Beijing, China. Chemosphere 92:435–444

    Article  CAS  Google Scholar 

  • Li X, Shi H, Li K, Zhang L, Gan Y (2014) Occurrence and fate of antibiotics in advanced wastewater treatment facilities and receiving rivers in Beijing, China. Front Environ Sci Eng 8:888–894. doi:10.1007/s11783-014-0735-0

    Article  CAS  Google Scholar 

  • Li B, Ju F, Cai L, Zhang T (2015a) Profile and fate of bacterial pathogens in sewage treatment plants revealed by high-throughput metagenomic approach. Environ Sci Technol 49:10492–10502

    Article  CAS  Google Scholar 

  • Li X, Shi H, Li K, Zhang L (2015b) Combined process of biofiltration and ozone oxidation as an advanced treatment process for wastewater reuse. Front Environ Sci Eng 9:1076–1083

    Article  CAS  Google Scholar 

  • Li J, Cheng W, Xu L, Jiao Y, Baig SA, Chen H (2016) Occurrence and removal of antibiotics and the corresponding resistance genes in wastewater treatment plants: effluents’ influence to downstream water environment. Environ Sci Pollut Res 23:6826–6835

    Article  CAS  Google Scholar 

  • Li N, Sheng G-P, Lu Y-Z, Zeng RJ, Yu H-Q (2017) Removal of antibiotic resistance genes from wastewater treatment plant effluent by coagulation. Water Res 111:204–212

    Article  CAS  Google Scholar 

  • Lindberg R, Jarnheimer PA, Olsen B, Johansson M, Tysklind M (2004) Determination of antibiotic substances in hospital sewage water using solid phase extraction and liquid chromatography/mass spectrometry and group analogue internal standards. Chemosphere 57:1479–1488

    Article  CAS  Google Scholar 

  • Liu G (2012) Nitrification performance of activated sludge under low dissolved oxygen conditions

  • Liu L, Hall G, Champagne P (2015) Effects of environmental factors on the disinfection performance of a wastewater stabilization pond operated in a temperate climate. Water 8:5

    Article  Google Scholar 

  • Lochan H, Moodley C, Rip D, Bamford C, Hendricks M, Davidson A, Eley B (2016) Emergence of vancomycin-resistant Enterococcus at a tertiary paediatric hospital in South Africa. S Afr Med J 106:562–566

    Article  Google Scholar 

  • Lone R, Syed K, Abdul R, Sheikh SA, Shah F (2009) Unusual case of methicillin resistant Staphylococcus aureus and Acanthamoeba keratitis in a non-contact lens wearer from Kashmir. India BMJ Case Rep. doi:10.1136/bcr.08.2008.0642

    Google Scholar 

  • Lu X et al (2015) Bacterial pathogens and community composition in advanced sewage treatment systems revealed by metagenomics analysis based on high-throughput sequencing. PLoS One 10:e0125549. doi:10.1371/journal.pone.0125549

    Article  CAS  Google Scholar 

  • Luczkiewicz A, Fudala-Ksiazek S, Jankowska K, Quant B, Olanczuk-Neyman K (2010) Diversity of fecal coliforms and their antimicrobial resistance patterns in wastewater treatment model plant. Water Sci Technol 61:1383–1392. doi:10.2166/wst.2010.015

    Article  CAS  Google Scholar 

  • MacKay AA, Canterbury B (2005) Oxytetracycline sorption to organic matter by metal-bridging. J Environ Qual 34:1964–1971

    Article  CAS  Google Scholar 

  • Magalhães MJTL et al (2016) Multidrug resistant Pseudomonas aeruginosa survey in a stream receiving effluents from ineffective wastewater hospital plants. BMC Microbiol 16:193. doi:10.1186/s12866-016-0798-0

    Article  Google Scholar 

  • Maheux AF et al (2013) Abilities of the mCP Agar method and CRENAME alpha toxin-specific real-time PCR assay to detect Clostridium perfringens spores in drinking water. Appl Environ Microbiol 79:7654–7661. doi:10.1128/aem.02791-13

    Article  CAS  Google Scholar 

  • Maisonneuve E, Gerdes K (2014) Molecular mechanisms underlying bacterial persisters. Cell 157:539–548. doi:10.1016/j.cell.2014.02.050

    Article  CAS  Google Scholar 

  • Mantilla-Calderon D, Hong P-Y (2017) Fate and persistence of a pathogenic NDM-1-positive Escherichia coli strain in anaerobic and aerobic sludge microcosms. Appl Environ Microbiol. doi:10.1128/aem.00640-17

    Google Scholar 

  • Manzetti S, Ghisi R (2014) The environmental release and fate of antibiotics. Marine Poll Bull 79:7–15. doi:10.1016/j.marpolbul.2014.01.005

    Article  CAS  Google Scholar 

  • Mao D et al (2015) Prevalence and proliferation of antibiotic resistance genes in two municipal wastewater treatment plants. Water Res 85:458–466. doi:10.1016/j.watres.2015.09.010

    Article  CAS  Google Scholar 

  • Marshall BM, Levy SB (2011) Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24:718–733. doi:10.1128/CMR.00002-11

    Article  CAS  Google Scholar 

  • Marshall BM, Ochieng DJ, Levy SB (2009) Commensals: underappreciated reservoir of antibiotic resistance. Microbe 4:231–238

    Google Scholar 

  • Marx C, Gunther N, Schubert S, Oertel R, Ahnert M, Krebs P, Kuehn V (2015) Mass flow of antibiotics in a wastewater treatment plant focusing on removal variations due to operational parameters. Sci Total Environ 538:779–788. doi:10.1016/j.scitotenv.2015.08.112

    Article  CAS  Google Scholar 

  • Matteelli A, Roggi A, Carvalho ACC (2014) Extensively drug-resistant tuberculosis: epidemiology and management. Clin Epidemiol 6:111–118. doi:10.2147/CLEP.S35839

    Article  Google Scholar 

  • Mazel D, Dychinco B, Webb VA, Davies J (1998) A Distinctive Class of Integron in the Vibrio cholerae Genome. Science 280:605–608

    Article  CAS  Google Scholar 

  • Mema V (2010) Impact of poorly maintained waste water and sewage treatment plants: lessons from South Africa. ReSource 12:60–65

    Google Scholar 

  • Miranda C et al (2015) Genotypic characteristics of multidrug-resistant Pseudomonas aeruginosa from hospital wastewater treatment plant in Rio de Janeiro Brazil. J Appl Microbiol 118:1276–1286

    Article  CAS  Google Scholar 

  • Missotten JAM, Michiels J, Degroote J, De Smet S (2015) Fermented liquid feed for pigs: an ancient technique for the future. J Anim Sci Biotechnol 6:4

    Article  CAS  Google Scholar 

  • Moges F, Endris M, Belyhun Y, Worku W (2014) Isolation and characterization of multiple drug resistance bacterial pathogens from waste water in hospital and non-hospital environments Northwest Ethiopia. BMC Res Notes 7:215

    Article  CAS  Google Scholar 

  • Muchesa P, Mwamba O, Barnard TG, Bartie C (2014) Detection of Free-Living Amoebae Using Amoebal Enrichment in a Wastewater Treatment Plant of Gauteng Province South Africa. BioMed Res Int 2014:10. doi:10.1155/2014/575297

    Article  Google Scholar 

  • Munir M, Wong K, Xagoraraki I (2011) Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Res 45:681–693

    Article  CAS  Google Scholar 

  • Mutuku Christopher (2017) Antibiotic resistance profiles among enteric bacteria isolated from wastewater in septic tanks. ASRJETS 27:1

    Google Scholar 

  • Nakada N, Shinohara H, Murata A, Kiri K, Managaki S, Sato N, Takada H (2007) Removal of selected pharmaceuticals and personal care products (PPCPs) and endocrine-disrupting chemicals (EDCs) during sand filtration and ozonation at a municipal sewage treatment plant. Water Res 41:4373–4382

    Article  CAS  Google Scholar 

  • Nakada N, Kiri K, Shinohara H, Harada A, Kuroda K, Takizawa S, Takada H (2008) Evaluation of pharmaceuticals and personal care products as water-soluble molecular markers of sewage. Environ. Sci Technol 42:6347–6353

    Article  CAS  Google Scholar 

  • Nanninga TA, Bisschops I, López E, Martínez-Ruiz JL, Murillo D, Essl L, Starkl M (2012) Discussion on sustainable water technologies for peri-urban areas of Mexico City: balancing urbanization and environmental conservation. Water 4:739–758

    Article  Google Scholar 

  • Nascimento MJ, Oliveira JS, Mexia JT (1991) Contribution for the study of new pathogenic indicators removal from waste stabilization pond in Portugal. Water Sci Technol 24:381–386

    Google Scholar 

  • Odjadjare E, Olaniran A (2015) Prevalence of antimicrobial resistant and virulent Salmonella spp. in treated effluent and receiving aquatic milieu of wastewater treatment plants in Durban, South Africa. Int J Environ Res Public Health 12:9692

    Article  CAS  Google Scholar 

  • Okoh AI, Sibanda T, Nongogo V, Adefisoye M, Olayemi OO, Nontongana N (2015) Prevalence and characterisation of non-cholerae Vibrio spp. in final effluents of wastewater treatment facilities in two districts of the Eastern Cape Province of South Africa: implications for public health. Environ Sci Pollut Res 22:2008–2017. doi:10.1007/s11356-014-3461-z

    Article  CAS  Google Scholar 

  • Olaniran AO, Nzimande SBT, Mkize NG (2015) Antimicrobial resistance and virulence signatures of Listeria and Aeromonas species recovered from treated wastewater effluent and receiving surface water in Durban South Africa. BMC Microbiol 15:1–10. doi:10.1186/s12866-015-0570-x

    Article  CAS  Google Scholar 

  • Omar K, Barnard T (2010) The occurrence of pathogenic Escherichia coli in South African wastewater treatment plants as detected by multiplex PCR. Water SA 36:172–176

    CAS  Google Scholar 

  • Onesios KM, Yu JT, Bouwer EJ (2009) Biodegradation and removal of pharmaceuticals and personal care products in treatment systems: a review. Biodegradation 20:441–466

    Article  CAS  Google Scholar 

  • Osei Sekyere J (2016) Current State of Resistance to Antibiotics of Last-Resort in South Africa: a review from a public health perspective. Front Public Health 4:209. doi:10.3389/fpubh.2016.00209

    Article  Google Scholar 

  • Osei Sekyere J, Govinden U, Bester LA, Essack SY (2016) Colistin and tigecycline resistance in Carbapenemase-producing gram negative bacteria: emerging resistance mechanisms and detection methods. J Appl Microbiol 121:601–617

    Article  CAS  Google Scholar 

  • Petrosino JF, Galhardo RS, Morales LD, Rosenberg SM (2009) Stress-induced β-Lactam antibiotic resistance mutation and sequences of stationary-phase mutations in the Escherichia coli chromosome. J Bacteriol 191:5881–5889. doi:10.1128/jb.00732-09

    Article  CAS  Google Scholar 

  • Popple T (2013) The behaviour, fate and removal of pharmaceuticals in biological nutrient removal sewage treatment. University of Portsmouth

  • Port JA, Cullen AC, Wallace JC, Smith MN, Faustman EM (2014) Metagenomic frameworks for monitoring antibiotic resistance in aquatic environments. Environ Health Perspect 122:222

    Article  Google Scholar 

  • Pruden A et al (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect 121:878

    Article  Google Scholar 

  • Qi F-F, Huang M-H, Zheng Y, Xu Q (2015) Optimization of an A2/O process for tetracycline removal via response surface methodology coupled with a Box-Behnken design. J Environ Sci Health A Tox Hazard Subst Environ Eng Part A 50:735–743. doi:10.1080/10934529.2015.1011981

    Article  CAS  Google Scholar 

  • Raboni M, Torretta V, Urbini G (2013) Influence of strong diurnal variations in sewage quality on the performance of biological denitrification in small community wastewater treatment plants (WWTPs). Sustainability 5:3679–3689

    Article  CAS  Google Scholar 

  • Radhouani H, Igrejas G, Gonçalves A, Estepa V, Sargo R, Torres C, Poeta P (2013) Molecular characterization of extended-spectrum-beta-lactamase-producing Escherichia coli isolates from red foxes in Portugal. Arch Microbiol 195:141–144. doi:10.1007/s00203-012-0853-7

    Article  CAS  Google Scholar 

  • Rahube TO, Viana LS, Koraimann G, Yost CK (2014) Characterization and comparative analysis of antibiotic resistance plasmids isolated from a wastewater treatment plant. Front Microbiol 5:558. doi:10.3389/fmicb.2014.00558

    Article  Google Scholar 

  • Reardon Sara (2015) Dramatic rise seen in antibiotic use: New report provides the most comprehensive picture yet of antibiotic use and resistance worldwide. Nat News. doi:10.1038/nature.2015.18383

    Google Scholar 

  • Reisner A, Wolinski H, Zechner EL (2012) In situ monitoring of IncF plasmid transfer on semi-solid agar surfaces reveals a limited invasion of plasmids in recipient colonies. Plasmid 67:155–161. doi:10.1016/j.plasmid.2012.01.001

    Article  CAS  Google Scholar 

  • Rizzo L, Fiorentino A, Anselmo A (2013a) Advanced treatment of urban wastewater by UV radiation: effect on antibiotics and antibiotic-resistant E. coli strains. Chemosphere 92:171–176

    Article  CAS  Google Scholar 

  • Rizzo L et al (2013b) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360

    Article  CAS  Google Scholar 

  • Rothrock MJ, Hiett KL, Kiepper BH, Ingram K, Hinton A (2013) Quantification of zoonotic bacterial pathogens within commercial poultry processing water samples using droplet digital PCR. Adv Microbiol 3:403–411

    Article  CAS  Google Scholar 

  • Sadowy E, Luczkiewicz A (2014) Drug-resistant and hospital-associated Enterococcus faecium from wastewater, riverine estuary and anthropogenically impacted marine catchment basin. BMC Microbiol 14:66. doi:10.1186/1471-2180-14-66

    Article  CAS  Google Scholar 

  • Santiago-Rodriguez T, Kinzelman J, Toranzos G (2016) Current and developing methods for the detection of microbial indicators in environmental freshwaters and drinking waters, p 3.1.1–1–3.1.1–10. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environ. Microbiol., 4th Ed. ASM Press, Washington. doi:10.1128/9781555818821.ch3.1

  • Saur T, Morin E, Habouzit F, Bernet N, Escudié R (2017) Impact of wall shear stress on initial bacterial adhesion in rotating annular reactor. PLoS One 12:e0172113

    Article  CAS  Google Scholar 

  • Schaaf HS et al. (1996) The 5-year outcome of multidrug resistant tuberculosis patients in the Cape Province of South Africa Tropical medicine and international health: TM & IH 1:718–722

  • Sengupta S, Chattopadhyay MK, Grossart HP (2013) The multifaceted roles of antibiotics and antibiotic resistance in nature. Front Microbiol 4:47. doi:10.3389/fmicb.2013.00047

    Article  Google Scholar 

  • Sewpacksa (2014) The reality of South Africa’s Wastewater Treatment Technology. Creamer Media Engineering News. Accesed 03/04/2017 http://www.engineeringnews.co.za/article/the-reality-of-south-africas-wastewater-treatment-technology-2014-04-22/rep_id:4136.

  • Shahzad M, Khan SJ, Paul P (2015) Influence of temperature on the performance of a full-scale activated sludge process operated at varying solids retention times whilst treating municipal sewage. Water 7:855–867

    Article  Google Scholar 

  • Sharma VK, Johnson N, Cizmas L, McDonald TJ, Kim H (2016) A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere 150:702–714

    Article  CAS  Google Scholar 

  • Sheludchenko M, Padovan A, Katouli M, Stratton H (2016) Removal of fecal indicators, pathogenic bacteria, Adenovirus, Cryptosporidium and Giardia (oo) cysts in waste stabilization ponds in Northern and Eastern Australia. Int J Environ Res Public Health 13:96

    Article  CAS  Google Scholar 

  • Shi P, Jia S, Zhang XX, Zhang T, Cheng S, Li A (2013) Metagenomic insights into chlorination effects on microbial antibiotic resistance in drinking water. Water Res 47:111–120

    Article  CAS  Google Scholar 

  • Shintani M et al (2014) Single-Cell Analyses revealed transfer ranges of IncP-1, IncP-7, and IncP-9 plasmids in a soil bacterial community. Appl Environ Microbiol 80:138–145. doi:10.1128/aem.02571-13

    Article  CAS  Google Scholar 

  • Siéliéchi JM et al (2008) Changes in humic acid conformation during coagulation with ferric chloride: Implications for drinking water treatment. Water Res 42:2111–2123

    Article  CAS  Google Scholar 

  • Singer AC et al (2014) Intra- and inter-pandemic variations of antiviral, antibiotics and decongestants in wastewater treatment plants and receiving rivers. PLoS One 9:e108621

    Article  CAS  Google Scholar 

  • Singer AC, Shaw H, Rhodes V, Hart A (2016) Review of antimicrobial resistance in the environment and its relevance to environmental regulators Front. Microbiol 7

  • Singh A, Poshtiban S, Evoy S (2013) Recent advances in bacteriophage based biosensors for food-borne pathogen detection. Sensors 13:1763–1786

    Article  CAS  Google Scholar 

  • Slekovec C, Plantin J, Cholley P, Thouverez M, Talon D, Bertrand X, Hocquet D (2012) Tracking down antibiotic-resistant Pseudomonas aeruginosa isolates in a wastewater network. PLoS One 7:e49300

    Article  CAS  Google Scholar 

  • Smalla K, Heuer H, Götz A, Niemeyer D, Krögerrecklenfort E, Tietze E (2000) Exogenous isolation of antibiotic resistance plasmids from piggery manure slurries reveals a high prevalence and diversity of IncQ-Like plasmids. Appl Environ Microbiol 66:4854–4862. doi:10.1128/aem.66.11.4854-4862.2000

    Article  CAS  Google Scholar 

  • Stoesser N et al (2013) Predicting antimicrobial susceptibilities for Escherichia coli and Klebsiella pneumoniae isolates using whole genomic sequence data. J Antimicrob Chemother 68:2234–2244. doi:10.1093/jac/dkt180

    Article  CAS  Google Scholar 

  • Sudhanandh V, Udayakumar P, Faisal A, Potty V, Ouseph P, Prasanthan V, Babu KN (2012) Distribution of potentially pathogenic enteric bacteria in coastal sea waters along the Southern Kerala coast, India. J Environ Bio 33:61

    CAS  Google Scholar 

  • Sukati BH (2012) The potential of biological sludge amended combustion coal ash residues as artificial plant growth media: a laboratory column study to assess the influence of weathering on elemental release. University of Pretoria, Pretoria

    Google Scholar 

  • Sun J, Li L, Liu B, Xia J, Liao X, Liu Y (2014) Development of aminoglycoside and β-lactamase resistance among intestinal microbiota of swine treated with lincomycin, chlortetracycline, and amoxicillin. Front Microbiol 5

  • Suzuki S, Horinouchi T, Furusawa C (2014) Prediction of antibiotic resistance by gene expression profiles Nature communications. 5

  • Szczepanowski R, Braun S, Riedel V, Schneiker S, Krahn I, Puhler A, Schluter A (2005) The 120 592 bp IncF plasmid pRSB107 isolated from a sewage-treatment plant encodes nine different antibiotic-resistance determinants, two iron-acquisition systems and other putative virulence-associated functions. Microbiology 151:1095–1111

    Article  CAS  Google Scholar 

  • Tang J et al (2016) Metagenomic analysis of bacterial community composition and antibiotic resistance genes in a wastewater treatment plant and its receiving surface water. Ecotoxicol Environ Saf 132:260–269

    Article  CAS  Google Scholar 

  • Thamdrup B, Fleischer S (1998) Temperature dependence of oxygen respiration, nitrogen mineralization, and nitrification in Arctic sediments. Aquat Microb Ecol 15:191–199

    Article  Google Scholar 

  • Thanner S, Drissner D, Walsh F (2016) Antimicrobial Resistance in Agriculture. MBio 7:e02227

    Article  CAS  Google Scholar 

  • Top E, De Smet I, Verstraete W, Dijkmans R, Mergeay M (1994) Exogenous Isolation of Mobilizing Plasmids from Polluted Soils and Sludges. Appl Environ Microbiol 60:831–839

    CAS  Google Scholar 

  • Torii N et al (2003) Spontaneous mutations in the Helicobacter pylori rpsL gene Mutat Res Genet Toxicol. Environ Mutagen 535:141–145. doi:10.1016/S1383-5718(02)00292-9

    Article  CAS  Google Scholar 

  • Torti A, Lever MA, Jørgensen BB (2015) Origin, dynamics, and implications of extracellular DNA pools in marine sediments Mar Genomics 24. Part 3:185–196

    Google Scholar 

  • Van Boeckel TP, Gandra SAA, Caudron Q, Grenfell BT, Levin SA, Laxminarayan Ramanan (2014a) Global antibiotic consumption 2000–2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14:745–750

    Google Scholar 

  • Van Boeckel TP, Gandra S, Ashok A, Caudron Q, Grenfell BT, Levin SA, Laxminarayan R (2014b) Global antibiotic consumption 2000–2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis 14:742–750

    Article  Google Scholar 

  • Van Boeckel TP et al (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci 112:5649–5654

    Article  CAS  Google Scholar 

  • van Elsas JD, McSpadden Gardener BB, Wolters AC, Smit E (1998) Isolation, Characterization, and Transfer of Cryptic Gene-Mobilizing Plasmids in the Wheat Rhizosphere. Appl Environ Microbiol 64:880–889

    Google Scholar 

  • Ventola CL (2015) The Antibiotic Resistance Crisis: Part 1: Causes and Threats. Pharm Therapeutics 40:277–283

    Google Scholar 

  • Vieno N, Sillanpää M (2014) Fate of diclofenac in municipal wastewater treatment plant—A review. Environ Int 69:28–39

    Article  CAS  Google Scholar 

  • Vieno N, Tuhkanen T, Kronberg L (2007) Elimination of pharmaceuticals in sewage treatment plants in Finland. Water Res 41:1001–1012. doi:10.1016/j.watres.2006.12.017

    Article  CAS  Google Scholar 

  • Walston SE (2013) Does increasing solids retention time during the wastewater treatment process affect the persistence of antibiotic resistance genes? The University of Arizona.

  • Wang S, Wang H (2015) Adsorption behavior of antibiotic in soil environment: a critical review. Front Environ Sci Eng 9:565–574. doi:10.1007/s11783-015-0801-2

    Article  CAS  Google Scholar 

  • Wang H et al (2014) Water and wastewater treatment in Africa-Current practices and challenges. Clean 42:1029–1035

    CAS  Google Scholar 

  • Wang D-N et al (2016) A new adsorption-elution technique for the concentration of aquatic extracellular antibiotic resistance genes from large volumes of water. Water Res 92:188–198

    Article  CAS  Google Scholar 

  • Wasserman S, Boyles T, Mendelson M (2014) A pocket guide to antibiotic prescribing for adults in South Africa, 2014

  • Wessels J, Ford W, Szymczak W, Schneider S (1998) The complexation of tetracycline and anhydrotetracycline with Mg2+ and Ca2+: a spectroscopic study. J Phys Chem B 102:9323–9331

    Article  CAS  Google Scholar 

  • Weyer K, Groenewald P, Zwarenstein M, Lombard CJ (1995) Tuberculosis drug resistance in the Western Cape. South Africa Med J 85:499–504

    CAS  Google Scholar 

  • WHO (2017) Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. WHO 2017:1–7

    Google Scholar 

  • Wisniewski C (2007) Membrane bioreactor for water reuse Desalination 203:15–19

    CAS  Google Scholar 

  • Wolters B, Kyselková M, Krögerrecklenfort E, Kreuzig R, Smalla K (2015) Transferable antibiotic resistance plasmids from biogas plant digestates often belong to the IncP-1ε subgroup. Front Microbiol. doi:10.3389/fmicb.2014.00765

    Google Scholar 

  • Woodford N, Ellington MJ (2007) The emergence of antibiotic resistance by mutation. Clin Microbiol Infect 13:5–18. doi:10.1111/j.1469-0691.2006.01492.x

    Article  CAS  Google Scholar 

  • Wright GD (2014) Something old, something new: revisiting natural products in antibiotic drug discovery. Can J Microbiol 60:147–154. doi:10.1139/cjm-2014-0063

    Article  CAS  Google Scholar 

  • Xiao F, Simcik MF, Gulliver JS (2013) Mechanisms for removal of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) from drinking water by conventional and enhanced coagulation. Water Res 47:49–56

    Article  CAS  Google Scholar 

  • Xu B, Mao D, Luo Y, Xu L (2011) Sulfamethoxazole biodegradation and biotransformation in the water–sediment system of a natural river. Bioresour Technol 102:7069–7076

    Article  CAS  Google Scholar 

  • Xu J et al (2015) Occurrence of antibiotics and antibiotic resistance genes in a sewage treatment plant and its effluent-receiving river. Chemosphere 119:1379–1385. doi:10.1016/j.chemosphere.2014.02.040

    Article  CAS  Google Scholar 

  • Yamamoto M et al (2013) Regional dissemination of Acinetobacter species harbouring metallo-β-lactamase genes in Japan. Clin Microbiol Infect 19:729–736

    Article  CAS  Google Scholar 

  • Yang Y, Li B, Ju F, Zhang T (2013) Exploring variation of antibiotic resistance genes in activated sludge over a four-Year period through a metagenomic approach. Environ Sci Technol 47:10197–10205

    Article  CAS  Google Scholar 

  • Yang Y, Li B, Zou S, Fang HHP, Zhang T (2014) Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res 62:97–106

    Article  CAS  Google Scholar 

  • Yang F, Mao D, Zhou H, Luo Y (2016) Prevalence and fate of carbapenemase genes in a wastewater treatment plant in Northern China. PLoS One 11:e0156383

    Article  CAS  Google Scholar 

  • Yuan Q-B, Guo M-T, Yang J (2015) Fate of antibiotic resistant bacteria and genes during wastewater chlorination: implication for antibiotic resistance control. PLoS One 10:e0119403

    Article  CAS  Google Scholar 

  • Zeng Q, Li Y, Yang S (2013) Sludge retention time as a suitable operational parameter to remove both estrogen and nutrients in an anaerobic–anoxic–aerobic activated sludge system. Environ Eng Sci 30:161–169

    Article  CAS  Google Scholar 

  • Zeng J, Zhao D, Yu Z, Huang R, Wu QL (2014) Temperature responses of ammonia-oxidizing prokaryotes in freshwater sediment microcosms. PLoS One 9:e100653

    Article  CAS  Google Scholar 

  • Zhang Y (2014) Persisters, persistent infections and the Yin-Yang model. Emerg Microbes Infect 3:e3

    Article  CAS  Google Scholar 

  • Zhang T (2016) Antibiotics and resistance genes in wastewater treatment plants. http://resistancecontrol.info/amr-in-food-water-and-the-environment/antibiotics-and-resistance-genes-in-wastewater-treatment-plants/

  • Zhang R, Vigneswaran S, Ngo HH, Nguyen H (2006) Magnetic ion exchange (MIEX) resin as a pre-treatment to a submerged membrane system in the treatment of biologically treated wastewater. Desalination 192:296–302

    Article  CAS  Google Scholar 

  • Zhang M, Visser S, Pereira e Silva MC, van Elsas JD (2015a) IncP-1 and PromA group plasmids are major providers of horizontal gene transfer capacities across bacteria in the mycosphere of different soil fungi. Microb Ecol 69:169–179. doi:10.1007/s00248-014-0482-6

    Article  CAS  Google Scholar 

  • Zhang S et al (2015b) Fate of antibiotic resistant cultivable heterotrophic bacteria and antibiotic resistance genes in wastewater treatment processe.s. Chemosphere 135:138–145

    Article  CAS  Google Scholar 

  • Zuccato E, Castiglioni S, Bagnati R, Melis M, Fanelli R (2010) Source, occurrence and fate of antibiotics in the Italian aquatic environment. J Hazard Mater 179:1042–1048. doi:10.1016/j.jhazmat.2010.03.110

    Article  CAS  Google Scholar 

  • Zyara AM, Torvinen E, Veijalainen A-M, Heinonen-Tanski H (2016) The effect of UV and combined chlorine/UV treatment on Coliphages in drinking water disinfection. Water 8:130

    Article  Google Scholar 

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Nnadozie, C.F., Kumari, S. & Bux, F. Status of pathogens, antibiotic resistance genes and antibiotic residues in wastewater treatment systems. Rev Environ Sci Biotechnol 16, 491–515 (2017). https://doi.org/10.1007/s11157-017-9438-x

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