Removal of antibiotic resistant bacteria and antibiotic resistance genes: a bibliometric review

Highlights

● A total of 3714 studies on ARB and ARGs removal techniques over 26 years were reviewed.

● Adsorption has been studied mostly for ARB and ARGs degradation, and adsorbents are important.

● Nanomaterials and biomodified materials exhibit great potential.

● Combined techniques to remove ARB and ARGs are proposed for the future.

Abstract

The spread of antibiotic resistance is a global threat, causing elevated death rates and economic costs. A growing number of studies have focused on the removal of antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARGs) in environmental settings. However, summaries and reviews of removal techniques are limited. This study examined publications on ARB and ARGs removal from 1998 to 2023 through a bibliometric approach based on the Web of Science database. Research progress during the past 26 years was analyzed by collecting annual publications, countries, journals and keywords. The number of articles related to the removal of ARB and ARGs has increased annually. The main types of ARB and ARGs, their environmental milieus and the most commonly studied removal techniques were summarized by keyword clustering. The results revealed that tetracycline- and sulfonamide-resistant bacteria are the ARB of greatest concern; that sul1, sul2, and tetA are the most frequently studied ARGs; and that municipal sewage and drinking water are the most studied ARB and ARGs transmission sites. For treatment techniques, adsorption technology is the most widely studied, and the selection of adsorption materials is particularly important, with nanomaterials and biomodified materials having great prospects for development. The combination of membrane filtration with advanced oxidation treatment or biodegradation technology is the most promising technology in this field. Our findings can inform future efforts to further reduce the distribution risks of antibiotic resistance and improve removal techniques.

Graphical abstract

Keywords

ARB / ARGs / Bibliometric / Keyword analysis / Removal techniques

References

[1] Abudureheman M, Ailijiang N, Mamat A, Feng Y, He C, Pu M. (2023). Enhanced biodegradation of fluoroquinolones and the changes of bacterial communities and antibiotic-resistant genes under intermittent electrical stimulation. Environmental Research, 219: 115127

[2] Ahmed Y, Zhong J, Yuan Z, Guo J. (2021). Simultaneous removal of antibiotic resistant bacteria, antibiotic resistance genes, and micropollutants by a modified photo-Fenton process. Water Research, 197: 117075

[3] Ajibade F O, Yin W X, Guadie A, Ajibade T F, Liu Y, Kumwimba M N, Liu W Z, Han J L, Wang H C, Wang A J. (2023). Impact of biochar amendment on antibiotic removal and ARGs accumulation in constructed wetlands for low C/N wastewater treatment. Chemical Engineering Journal, 459: 141541

[4] Anderson M, Schulze K, Cassini A, Plachouras D, Mossialos E. (2019). A governance framework for development and assessment of national action plans on antimicrobial resistance. Lancet. Infectious Diseases, 19(11): E371–E384

[5] Ashraf A, Liu G, Arif M, Mian M M, Rashid A, Yousaf B, Khawar M I, Riaz L, Safeer R. (2022). Insights into the synthesis and application of biochar assisted graphene-based materials in antibiotic remediation. Journal of Cleaner Production, 361: 132211

[6] Band V I, Hufnagel D A, Jaggavarapu S, Sherman E X, Wozniak J E, Satola S W, Farley M M, Jacob J T, Burd E M, Weiss D S. (2019). Antibiotic combinations that exploit heteroresistance to multiple drugs effectively control infection. Nature Microbiology, 4(10): 1627–1635

[7] Baggs J, Fridkin S K, Pollack L A, Srinivasan A, Jernigan J A. (2016). Estimating national trends in inpatient antibiotic use among US hospitals from 2006 to 2012. JAMA Internal Medicine, 176(11): 1639–1648

[8] Baker S, Thomson N, Weill F X, Holt K E. (2018). Genomic insights into the emergence and spread of antimicrobial-resistant bacterial pathogens. Science, 360(6390): 733–738

[9] Barrasa-Villar J I, Aibar-Remón C, Prieto-Andrés P, Mareca-Doñate R, Moliner-Lahoz J. (2017). Impact on morbidity, mortality, and length of stay of hospital-acquired infections by resistant microorganisms. Nephrology, Dialysis, Transplantation, 65(4): 644–652

[10] Batt AL, Snow DD, Aga DS. (2006). Occurrence of sulfonamide antimicrobials in private water wells in Washington County, Idaho, USA. Chemosphere: Environmental Toxicology and Risk Assessment, 64(11): 1963–1971

[11] Ben Y, Fu C, Hu M, Liu L, Wong M H, Zheng C. (2019). Human health risk assessment of antibiotic resistance associated with antibiotic residues in the environment: a review. Environmental Research, 169: 483–493

[12] Bonetta S, Di Cesare A, Pignata C, Sabatino R, Macrì M, Corno G, Panizzolo M, Bonetta S, Carraro E. (2022). Occurrence of antibiotic-resistant bacteria and resistance genes in the urban water cycle. Environmental Science and Pollution Research International, 30(12): 35294–35306

[13] Bouki C, Venieri D, Diamadopoulos E. (2013). Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: a review. Ecotoxicology and Environmental Safety, 91: 1–9

[14] Brito I L. (2021). Examining horizontal gene transfer in microbial communities. Nature Reviews. Microbiology, 19(7): 442–453

[15] Brown K D, Kulis J, Thomson B, Chapman T H, Mawhinney D B. (2006). Occurrence of antibiotics in hospital, residential, and dairy effluent, municipal wastewater, and the Rio Grande in New Mexico. Science of the Total Environment, 366(2−3): 772–783

[16] Chen C, Li C, Reniers G, Yang F. (2021). Safety and security of oil and gas pipeline transportation: a systematic analysis of research trends and future needs using WoS. Journal of Cleaner Production, 279: 123583

[17] Chen Y, Jin Q, Fang H, Lei H, Hu J, Wu Y, Chen J, Wang C, Wan Y. (2019). Analytic network process: academic insights and perspectives analysis. Journal of Cleaner Production, 235: 1276–1294

[18] Cuetero-MartínezYFlores-RamírezAde los Cobos-Vasconcelos DAguirre-Garrido J FLópez-VidalY NoyolaA (2023). Removal of bacterial pathogens and antibiotic resistance bacteria by anaerobic sludge digestion with thermal hydrolysis pre-treatment and alkaline stabilization post-treatment. Chemosphere, 313

[19] Dey D, Chowdhury S, Sen R. (2023). Insight into recent advances on nanotechnology-mediated removal of antibiotic resistant bacteria and genes. Journal of Water Process Engineering, 52: 103535

[20] Diem A, Wolter S C. (2013). The use of bibliometrics to measure research performance in education sciences. Research in Higher Education, 54(1): 86–114

[21] Ding X, Yang Z. (2022). Knowledge mapping of platform research: a visual analysis using VOSviewer and CiteSpace. Electronic Commerce Research, 22(3): 787–809

[22] Dires S, Birhanu T, Ambelu A, Sahilu G. (2018). Antibiotic resistant bacteria removal of subsurface flow constructed wetlands from hospital wastewater. Journal of Environmental Chemical Engineering, 6(4): 4265–4272

[23] Duan R, Ma S, Xu S, Wang B, He M, Li G, Fu H, Zhao P. (2022). Soybean straw biochar activating peroxydisulfate to simultaneously eliminate tetracycline and tetracycline resistance bacteria: Insights on the mechanism. Water Research, 218: 118489

[24] Fahimnia B, Sarkis J, Davarzani H. (2015). Green supply chain management: a review and bibliometric analysis. International Journal of Production Economics, 162: 101–114

[25] Fiorentino A, Esteban B, Garrido-Cardenas J A, Kowalska K, Rizzo L, Aguera A, Pérez J A S. (2019). Effect of solar photo-Fenton process in raceway pond reactors at neutral pH on antibiotic resistance determinants in secondary treated urban wastewater. Journal of Hazardous Materials, 378: 120737

[26] Gao F Z, Zou H Y, Wu D L, Chen S, He L Y, Zhang M, Bai H, Ying G G. (2020). Swine farming elevated the proliferation of Acinetobacter with the prevalence of antibiotic resistance genes in the groundwater. Environment International, 136: 105484

[27] Gao P, Mao D, Luo Y, Wang L, Xu B, Xu L. (2012). Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Research, 46(7): 2355–2364

[28] Giannakis S, Polo Lopez M I, Spuhler D, Sanchez Perez J A, Fernandez Ibanez P, Pulgarin C. (2016). Solar disinfection is an augmentable, in situ-generated photo-Fenton reaction-Part 1: A review of the mechanisms and the fundamental aspects of the process. Applied Catalysis B: Environmental, 199: 199–223

[29] Guo C, Wang K, Hou S, Wan L, Lv J, Zhang Y, Qu X, Chen S, Xu J. (2017). H₂O₂ and/or TiO₂ photocatalysis under UV irradiation for the removal of antibiotic resistant bacteria and their antibiotic resistance genes. Journal of Hazardous Materials, 323: 710–718

[30] Guo N, Wang Y, Tong T, Wang S. (2018). The fate of antibiotic resistance genes and their potential hosts during bio-electrochemical treatment of high-salinity pharmaceutical wastewater. Water Research, 133: 79–86

[31] Gurmessa B, Pedretti E F, Cocco S, Cardelli V, Corti G. (2020). Manure anaerobic digestion effects and the role of pre- and post-treatments on veterinary antibiotics and antibiotic resistance genes removal efficiency. Science of the Total Environment, 721: 137532

[32] Hassoun-Kheir N, Stabholz Y, Kreft J U, de la Cruz R, Romalde J L, Nesme J, Sorensen S J, Smets B F, Graham D, Paul M. (2020). Comparison of antibiotic-resistant bacteria and antibiotic resistance genes abundance in hospital and community wastewater: a systematic review. Science of the Total Environment, 743: 140804

[33] He Y, Yin X, Li F, Wu B, Zhu L, Ge D, Wang N, Chen A, Zhang L, Yan B. . (2023). Response characteristics of antibiotic resistance genes and bacterial communities during agricultural waste composting: focusing on biogas residue combined with biochar amendments. Bioresource Technology, 372: 128636

[34] Hembach N, Alexander J, Hiller C, Wieland A, Schwartz T. (2019). Dissemination prevention of antibiotic resistant and facultative pathogenic bacteria by ultrafiltration and ozone treatment at an urban wastewater treatment plant. Scientific Reports, 9(1): 12843

[35] Honda R, Tachi C, Yasuda K, Hirata T, Noguchi M, Hara-Yamamura H, Yamamoto-Ikemoto R, Watanabe T. (2020). Estimated discharge of antibiotic-resistant bacteria from combined sewer overflows of urban sewage system. NPJ Clean Water, 3(1): 15

[36] Hossain . (2022). Antibiotics, antibiotic-resistant bacteria, and resistance genes in aquaculture: risks, current concern, and future thinking. Environmental Science and Pollution Research International, 29(8): 11054–11075

[37] Iakovides I C, Michael-Kordatou I, Moreira N F F, Ribeiro A R, Fernandes T, Pereira M F R, Nunes O C, Manaia C M, Silva A M T, Fatta-Kassinos D. (2019). Continuous ozonation of urban wastewater: removal of antibiotics, antibiotic-resistant Escherichia coli and antibiotic resistance genes and phytotoxicity. Water Research, 159: 333–347

[38] Kampouris I D, Alygizakis N, Klümper U, Agrawal S, Lackner S, Cacace D, Kunze S, Thomaidis N S, Slobdonik J, Berendonk T U. (2022). Elevated levels of antibiotic resistance in groundwater during treated wastewater irrigation associated with infiltration and accumulation of antibiotic residues. Journal of Hazardous Materials, 423: 127155

[39] Karaolia P, Michael-Kordatou I, Hapeshi E, Drosou C, Bertakis Y, Christofilos D, Armatas G S, Sygellou L, Schwartz T, Xekoukoulotakis N P. . (2018). Removal of antibiotics, antibiotic-resistant bacteria and their associated genes by graphene-based TiO₂ composite photocatalysts under solar radiation in urban wastewaters. Applied Catalysis B: Environmental, 224: 810–824

[40] Korzeniewska E, Korzeniewska A, Harnisz M. (2013). Antibiotic resistant Escherichia coli in hospital and municipal sewage and their emission to the environment. Ecotoxicology and Environmental Safety, 91: 96–102

[41] Kumar V, Jaiswal K K, Verma M, Vlaskin M S, Nanda M, Chauhan P K, Singh A, Kim H. (2021). Algae-based sustainable approach for simultaneous removal of micropollutants, and bacteria from urban wastewater and its real-time reuse for aquaculture. Science of the Total Environment, 774: 145556

[42] Kümmerer K. (2009). Antibiotics in the aquatic environment: a review-Part II. Chemosphere, 75(4): 435–441

[43] Lan L, Kong X, Sun H, Li C, Liu D. (2019). High removal efficiency of antibiotic resistance genes in swine wastewater via nanofiltration and reverse osmosis processes. Journal of Environmental Management, 231: 439–445

[44] Le T H, Ng C, Tran N H, Chen H, Gin K Y H. (2018). Removal of antibiotic residues, antibiotic resistant bacteria and antibiotic resistance genes in municipal wastewater by membrane bioreactor systems. Water Research, 145: 498–508

[45] Liang J H, Gao P, Li B H, Kang L F, Feng L, Han Q, Liu Y Z, Zhang L Q. (2022). Characteristics of typical dissolved black carbons and their influence on the formation of disinfection by-products in chlor(am)ination. Frontiers of Environmental Science & Engineering, 16(12): 150

[46] Li B, Qiu Y, Li J, Liang P, Huang X. (2019a). Removal of antibiotic resistance genes in four full-scale membrane bioreactors. Science of the Total Environment, 653: 112–119

[47] Li F, Zhu J, Sun P, Zhang M, Li Z, Xu D, Gong X, Zou X, Geim A K, Su Y. . (2022a). Highly efficient and selective extraction of gold by reduced graphene oxide. Nature Communications, 13(1): 4472

[48] Li J, Cheng W, Xu L, Strong P J, Chen H. (2015). Antibiotic-resistant genes and antibiotic-resistant bacteria in the effluent of urban residential areas, hospitals, and a municipal wastewater treatment plant system. Environmental Science and Pollution Research International, 22(6): 4587–4596

[49] Li J, Ren S, Qiu X, Zhao S, Wang R, Wang Y. (2022b). Electroactive ultrafiltration membrane for simultaneous removal of antibiotic, antibiotic resistant bacteria, and antibiotic resistance genes from wastewater effluent. Environmental Science & Technology, 56(21): 15120–15129

[50] Li S, Zhang R, Hu J, Shi W, Kuang Y, Guo X, Sun W. (2019b). Occurrence and removal of antibiotics and antibiotic resistance genes in natural and constructed riverine wetlands in Beijing, China. Science of the Total Environment, 664: 546–553

[51] Li W, Yang Z, Hu J, Wang B, Rong H, Li Z, Sun Y, Wang Y, Zhang X, Wang M. . (2022c). Evaluation of culturable “last-resort” antibiotic resistant pathogens in hospital wastewater and implications on the risks of nosocomial antimicrobial resistance prevalence. Journal of Hazardous Materials, 438: 129477

[52] Liu X, Guo X, Liu Y, Lu S, Xi B, Zhang J, Wang Z, Bi B. (2019). A review on removing antibiotics and antibiotic resistance genes from wastewater by constructed wetlands: performance and microbial response. Environmental Pollution, 254: 112996

[53] Liu X, Zhao S, Tan L, Tan Y, Wang Y, Ye Z, Hou C, Xu Y, Liu S, Wang G. (2022). Frontier and hot topics in electrochemiluminescence sensing technology based on CiteSpace bibliometric analysis. Biosensors & Bioelectronics, 201: 113932

[54] Lu J, Wang Y, Li J, Mao L, Nguyen S H, Duarte T, Coin L, Bond P, Yuan Z, Guo J. (2018). Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera. Environment International, 121: 1217–1226

[55] Mailler R, Gasperi J, Coquet Y, Derome C, Buleté A, Vulliet E, Bressy A, Varrault G, Chebbo G, Rocher V. (2016). Removal of emerging micropollutants from wastewater by activated carbon adsorption: experimental study of different activated carbons and factors influencing the adsorption of micropollutants in wastewater. Journal of Environmental Chemical Engineering, 4(1): 1102–1109

[56] Masud M A A, Shin W S, Sarker A, Septian A, Das K, Deepo D M, Iqbal M A, Islam A R M T, Malafaia G. (2023). A critical review of sustainable application of biochar for green remediation: Research uncertainty and future directions. Science of the Total Environment, 904: 166813

[57] Michael S G, Michael-Kordatou I, Beretsou V G, Jäger T, Michael C, Schwartz T, Fatta-Kassinos D. (2019). Solar photo-Fenton oxidation followed by adsorption on activated carbon for the minimisation of antibiotic resistance determinants and toxicity present in urban wastewater. Applied Catalysis B: Environmental, 244: 871–880

[58] MirandaA C, Lepretti M, RizzoL, CaputoI, VaianoV, SaccoO, Lopes W S, SanninoD (2016). Surface water disinfection by chlorination and advanced oxidation processes: inactivation of an antibiotic resistant E. coli strain and cytotoxicity evaluation. Science of the Total Environment, 554–554: 1–6

[59] 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 Research, 45(2): 681–693

[60] Niu L, Liu W, Juhasz A, Chen J, Ma L. (2022). Emerging contaminants antibiotic resistance genes and microplastics in the environment: introduction to 21 review articles published in CREST during 2018–2022. Critical Reviews in Environmental Science and Technology, 52(23): 4135–4146

[61] O’Flaherty E, Borrego C M, Balcazar J L, Cummins E. (2018). Human exposure assessment to antibiotic-resistant Escherichia coli through drinking water. Science of the Total Environment, 616-617: 1356–1364

[62] O’Flaherty E, Solimini A G, Pantanella F, de Giusti M, Cummins E. (2019). Human exposure to antibiotic resistant-Escherichia coli through irrigated lettuce. Environment International, 122: 270–280

[63] Okeke I N, Laxminarayan R, Bhutta Z A, Duse A G, Jenkins P, O’Brien T F, Pablos-Mendez A, Klugman K P. (2005). Antimicrobial resistance in developing countries. Part I: Recent trends and current status. Lancet. Infectious Diseases, 5(8): 481–493

[64] Oliveira M, Leonardo I C, Silva A F, Crespo J G, Nunes M, Crespo M T B. (2022). Nanofiltration as an efficient tertiary wastewater treatment: elimination of total bacteria and antibiotic resistance genes from the discharged effluent of a full-scale wastewater treatment plant. Antibiotics (Basel, Switzerland), 11(5): 630

[65] Pazda M, Kumirska J, Stepnowski P, Mulkiewicz E. (2019). Antibiotic resistance genes identified in wastewater treatment plant systems: a review. Science of the Total Environment, 697: 134023

[66] Pei M, Zhang B, He Y, Su J, Gin K, Lev O, Shen G, Hu S. (2019). State of the art of tertiary treatment technologies for controlling antibiotic resistance in wastewater treatment plants. Environment International, 131: 105026

[67] Raichur A, Sinha N. (2023). Synthesis of multi-layered nanoswabs for simultaneous and expeditious removal of antibiotic-resistant bacteria, dyes, and antibiotics from wastewater. Separation and Purification Technology, 308: 122830

[68] Ravasi D, König R, Principi P, Perale G, Demarta A. (2019). Effect of powdered activated carbon as advanced step in wastewater treatments on antibiotic resistant microorganisms. Current Pharmaceutical Biotechnology, 20(1): 63–75

[69] Ren S, Boo C, Guo N, Wang S, Elimelech M, Wang Y. (2018). Photocatalytic reactive ultrafiltration membrane for removal of antibiotic resistant bacteria and antibiotic resistance genes from wastewater effluent. Environmental Science & Technology, 52(15): 8666–8673

[70] Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy M C, Michael I, Fatta-Kassinos D. (2013). Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Science of the Total Environment, 447: 345–360

[71] Rogers B A, Aminzadeh Z, Hayashi Y, Paterson D L. (2011). Country-to-country transfer of patients and the risk of multi-resistant bacterial infection. Clinical Infectious Diseases, 53(1): 49–56

[72] Rozman U, Duh D, Cimerman M, Turk S S. (2020). Hospital wastewater effluent: hot spot for antibiotic resistant bacteria. Journal of Water, Sanitation, and Hygiene for Development: a Journal of the International Water Association, 10(2): 171–178

[73] Shao B, Liu Z, Tang L, Liu Y, Liang Q, Wu T, Pan Y, Zhang X, Tan X, Yu J. (2022). The effects of biochar on antibiotic resistance genes (ARGs) removal during different environmental governance processes: a review. Journal of Hazardous Materials, 435: 129067

[74] Slipko K, Reif D, Schaar H, Saracevic E, Klinger A, Wallmann L, Krampe J, Woegerbauer M, Hufnagl P, Kreuzinger N. (2022). Advanced wastewater treatment with ozonation and granular activated carbon filtration: inactivation of antibiotic resistance targets in a long-term pilot study. Journal of Hazardous Materials, 438: 129396

[75] Slipko K, Reif D, Wögerbauer M, Hufnagl P, Krampe J, Kreuzinger N. (2019). Removal of extracellular free DNA and antibiotic resistance genes from water and wastewater by membranes ranging from microfiltration to reverse osmosis. Water Research, 164: 114916

[76] Stange C, Sidhu J P S, Toze S, Tiehm A. (2019). Comparative removal of antibiotic resistance genes during chlorination, ozonation, and UV treatment. International Journal of Hygiene and Environmental Health, 222(3): 541–548

[77] Suzuki S, Nakanishi S, Tamminen M, Yokokawa T, Sato-Takabe Y, Ohta K, Chou H Y, Muziasari W I, Virta M. (2019). Occurrence of sul and tet(M) genes in bacterial community in Japanese marine aquaculture environment throughout the year: profile comparison with Taiwan residents and Finnish aquaculture waters. Science of the Total Environment, 669: 649–656

[78] Tan H, Li J, He M, Li J, Zhi D, Qin F, Zhang C. (2021). Global evolution of research on green energy and environmental technologies: a bibliometric study. Journal of Environmental Management, 297: 113382

[79] Thelwall M. (2008). Bibliometrics to webometrics. Journal of Information Science, 34(4): 605–621

[80] Van den Bergh B, Michiels J E, Wenseleers T, Windels E M, Boer P V, Kestemont D, de Meester L, Verstrepen K J, Verstraeten N, Fauvart M. . (2016). Frequency of antibiotic application drives rapid evolutionary adaptation of Escherichia coli persistence. Nature Microbiology, 1(5): 16020

[81] Vikesland P, Garner E, Gupta S, Kang S, Maile-Moskowitz A, Zhu N. (2019). Differential drivers of antimicrobial resistance across the world. Accounts of Chemical Research, 52(4): 916–924

[82] Villar-Navarro E, Levchuk I, Rueda-Márquez J J, Homola T, Moriñigo M Á, Vahala R, Manzano M. (2021). Inactivation of simulated aquaculture stream bacteria at low temperature using advanced UVA- and solar-based oxidation methods. Solar Energy, 227: 477–489

[83] Voigt A M, Ciorba P, Döhla M, Exner M, Felder C, Lenz-Plet F, Sib E, Skutlarek D, Schmithausen R M, Faerber H A. (2020). The investigation of antibiotic residues, antibiotic resistance genes and antibiotic-resistant organisms in a drinking water reservoir system in Germany. International Journal of Hygiene and Environmental Health, 224: 113449

[84] Völker J, Stapf M, Miehe U, Wagner M. (2019). Systematic review of toxicity removal by advanced wastewater treatment Technologies via ozonation and activated carbon. Environmental Science & Technology, 53(13): 7215–7233

[85] Wang J, Chen X. (2022). Removal of antibiotic resistance genes (ARGs) in various wastewater treatment processes: an overview. Critical Reviews in Environmental Science and Technology, 52(4): 571–630

[86] Wang J, Wang S. (2019). Preparation, modification and environmental application of biochar: a review. Journal of Cleaner Production, 227: 1002–1022

[87] Wang J, Zhuan R. (2020). Degradation of antibiotics by advanced oxidation processes: an overview. Science of the Total Environment, 701: 135023

[88] Wang J H, Lu J, Wu J, Zhang Y, Zhang C. (2019a). Proliferation of antibiotic resistance genes in coastal recirculating mariculture system. Environmental Pollution, 248: 462–470

[89] Wang S, Ma X, Liu Y, Yi X, Du G, Li J. (2020a). Fate of antibiotics, antibiotic-resistant bacteria, and cell-free antibiotic-resistant genes in full-scale membrane bioreactor wastewater treatment plants. Bioresource Technology, 302: 122825

[90] Wang Y, Lu J, Engelstädter J, Zhang S, Ding B, P L K, Mao Z G, Yuan P L, Bond J H. (2020b). Non-antibiotic pharmaceuticals enhance the transmission of exogenous antibiotic resistance genes through bacterial transformation. ISME Journal, 14(8): 2179–2196

[91] Wang Y, Lu J, Mao L, Li J, Yuan Z, Bond P L, Guo J. (2019b). Antiepileptic drug carbamazepine promotes horizontal transfer of plasmid-borne multi-antibiotic resistance genes within and across bacterial genera. ISME Journal, 13(2): 509–522

[92] Wang Y, Lu J, Zhang S, Li J, Mao L K, Yuan Z G, Bond P L, Guo J H. (2021). Non-antibiotic pharmaceuticals promote the transmission of multidrug resistance plasmids through intra- and intergenera conjugation. ISME Journal, 15(9): 2493–2508

[93] Wang Y, Wang C, Yan S, Li Y, Cai C, Liu H, Ren P, Wang M, Kuang S. (2023a). The removal of antibiotic, antibiotic resistant bacteria and genes in persulfate oxidation system via activating by antibiotic fermentation dregs derived biochar. Journal of Cleaner Production, 394: 136328

[94] Wang Y, Yu Z G, Ding P B, Lu J, Mao L K, Ngiam L, Yuan Z G, Engelstädter J, Schembri M A, Guo J H. (2023b). Antidepressants can induce mutation and enhance persistence toward multiple antibiotics. Proceedings of the National Academy of Sciences of the United States of America, 120(5): e2208344120

[95] Wang Z, Zhang H, Han J, Xing H, Wu M, Yang T. (2017). Deadly sins of antibiotic abuse in china. Infection Control and Hospital Epidemiology, 38(6): 758–759

[96] Wu C, Fu L, Li H, Liu X, Wan C. (2022). Using biochar to strengthen the removal of antibiotic resistance genes: performance and mechanism. Science of the Total Environment, 816: 151554

[97] Xiong Q, Hu L X, Liu Y S, Zhao J L, He L Y, Ying G G. (2021). Microalgae-based technology for antibiotics removal: from mechanisms to application of innovational hybrid systems. Environment International, 155: 106594

[98] Yan R, Wang Y, Li J, Wang X, Wang Y. (2022). Determination of the lower limits of antibiotic biodegradation and the fate of antibiotic resistant genes in activated sludge: both nitrifying bacteria and heterotrophic bacteria matter. Journal of Hazardous Materials, 425: 127764

[99] Yao S, Hu Y, Ye J, Xie J, Zhao X, Liu L, Lyu S, Lin K, Cui C. (2022). Disinfection and mechanism of super-resistant Acinetobacter sp. and the plasmid-encoded antibiotic resistance gene bla(NDM-1) by UV/peroxymonosulfate. Chemical Engineering Journal, 433: 133565

[100] Yi M L, Fang Y, Hu G P, Liu S F, Ni J R, Liu T. (2022). Distinct community assembly processes underlie significant spatiotemporal dynamics of abundant and rare bacterioplankton in the Yangtze River. Frontiers of Environmental Science & Engineering, 16(6): 79

[101] Yu P, Zhou X, Li Z, Yan Y. (2020). Inactivation and change of tetracycline-resistant Escherichia coli in secondary effluent by visible light-driven photocatalytic process using Ag/AgBr/g-C₃N₄. Science of the Total Environment, 705: 135639

[102] Yu W, Zhan S, Shen Z, Zhou Q, Yang D. (2017). Efficient removal mechanism for antibiotic resistance genes from aquatic environments by graphene oxide nanosheet. Chemical Engineering Journal, 313: 836–846

[103] Yu Z, Wang Y, Lu J, Bond P L, Guo J. (2021). Nonnutritive sweeteners can promote the dissemination of antibiotic resistance through conjugative gene transfer. ISME Journal, 15(7): 2117–2130

[104] Yuan X R, Cui K P, Chen Y H, Wu S Y, Zhang Y, Liu T. (2023). Response of antibiotic and heavy metal resistance genes to the co-occurrence of gadolinium and sulfamethoxazole in activated sludge systems. Frontiers of Environmental Science & Engineering, 17(12): 154

[105] Zainab S M, Junaid M, Xu N, Malik R N. (2020). Antibiotics and antibiotic resistant genes (ARGs) in groundwater: a global review on dissemination, sources, interactions, environmental and human health risks. Water Research, 187: 116455

[106] Zhan H, Wang Y, Mi X, Zhou Z, Wang P, Zhou Q. (2020). Effect of graphitic carbon nitride powders on adsorption removal of antibiotic resistance genes from water. Chinese Chemical Letters, 31(10): 2843–2848

[107] Zhang M, Chen Q, Zhang R, Zhang Y, Wang F, He M, Guo X, Yang J, Zhang X, Mu J. (2023). Pyrolysis of Ca/Fe-rich antibiotic fermentation residues into biochars for efficient phosphate removal/recovery from wastewater: turning hazardous waste to phosphorous fertilizer. Science of the Total Environment, 869: 161732

[108] Zhang ML, Chen S, Yu X, Vikesland P, Pruden A. (2019a). Degradation of extracellular genomic, plasmid DNA and specific antibiotic resistance genes by chlorination. Frontiers of Environmental Science & Engineering, 13(3): 38

[109] Zhang S, Wang Y, Song H, Lu J, Yuan Z, Guo J. (2019b). Copper nanoparticles and copper ions promote horizontal transfer of plasmid-mediated multi-antibiotic resistance genes across bacterial genera. Environment International, 129: 478–487

[110] Zhang T, Hu Y, Jiang L, Yao S, Lin K, Zhou Y, Cui C. (2019c). Removal of antibiotic resistance genes and control of horizontal transfer risk by UV, chlorination and UV/chlorination treatments of drinking water. Chemical Engineering Journal, 358: 589–597

[111] Zhang W Z, Gao J F, Duan W J, Zhang D, Jia J X, Wang Y W. (2020). Sulfidated nanoscale zero-valent iron is an efficient material for the removal and regrowth inhibition of antibiotic resistance genes. Environmental Pollution, 263: 114508

[112] Zhang Z Y, Zhang Q, Wang T Z, Xu N H, Lu T, Hong W J, Penuelas J, Gillings M, Wang M X, Gao W W. . (2022). Assessment of global health risk of antibiotic resistance genes. Nature Communications, 13(1): 1553

[113] Zhao Y, Zhang C, Yang Z, Yang Y, Huang N, Arku J E, Mao G, Wang Y. (2021). Global trends and prospects in the removal of pharmaceuticals and personal care products: a bibliometric analysis. Journal of Water Process Engineering, 41: 102004

[114] Zhou C, Wu J, Dong L, Liu B, Xing D, Yang S, Wu X, Wang Q, Fan J, Feng L, Cao G. (2020). Removal of antibiotic resistant bacteria and antibiotic resistance genes in wastewater effluent by UV-activated persulfate. Journal of Hazardous Materials, 388: 122070

[115] Zhou Y, Leong S Y, Li Q. (2023). Modified biochar for removal of antibiotics and antibiotic resistance genes in the aqueous environment: a review. Journal of Water Process Engineering, 55: 104222

[116] Zhuang Y, Ren H, Geng J, Zhang Y, Zhang Y, Ding L, Xu K. (2015). Inactivation of antibiotic resistance genes in municipal wastewater by chlorination, ultraviolet, and ozonation disinfection. Environmental Science and Pollution Research International, 22(9): 7037–7044

Acknowledgements

We are grateful for the cooperation and participation of the utilities that were involved, which is supported by the National Natural Science Foundation of China (No. 42307529), the Hebei Natural Science Foundation (Nos. C2023110006 and E2023110001), the Research Fund of Tianjin Key Laboratory of Aquatic Science and Technology (TJKLAST-PT-2021-04), and the Cangzhou Institute of Tiangong University (No. TGCYY-F-0103).

Conflict of Interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-024-1906-2 and is accessible for authorized users.

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