Inactivation and risk control of pathogenic microorganisms in municipal sludge treatment: A review

Abstract

• Diversity and detection methods of pathogenic microorganisms in sludge.

• Control performance of sludge treatment processes on pathogenic microorganisms.

• Risk of pathogen exposure in sludge treatment and land application.

The rapid global spread of coronavirus disease 2019 (COVID-19) has promoted concern over human pathogens and their significant threats to public health security. The monitoring and control of human pathogens in public sanitation and health facilities are of great importance. Excessive sludge is an inevitable byproduct of sewage that contains human and animal feces in wastewater treatment plants (WWTPs). It is an important sink of different pollutants and pathogens, and the proper treatment and disposal of sludge are important to minimize potential risks to the environment and public health. However, there is a lack of comprehensive analysis of the diversity, exposure risks, assessment methods and inactivation techniques of pathogenic microorganisms in sludge. Based on this consideration, this review summarizes the control performance of pathogenic microorganisms such as enterovirus, Salmonella spp., and Escherichia coli by different sludge treatment technologies, including composting, anaerobic digestion, aerobic digestion, and microwave irradiation, and the mechanisms of pathogenic microorganism inactivation in sludge treatment processes are discussed. Additionally, this study reviews the diversity, detection methods, and exposure risks of pathogenic microorganisms in sludge. This review advances the quantitative assessment of pathogenic microorganism risks involved in sludge reuse and is practically valuable to optimize the treatment and disposal of sludge for pathogenic microorganism control.

Graphical abstract

Keywords

Sludge treatment / Pathogenic microorganisms / Inactivation mechanisms / Exposure risks / Land application

References

[1] Afolabi O O D, Sohail M (2017). Microwaving human faecal sludge as a viable sanitation technology option for treatment and value recovery: A critical review. Journal of Environmental Management, 187: 401–415

[2] AL-Ghonaiem M I, Ibrahim A S S, Al-Salamah A A (2010). Application of gamma irradiation in treatment of waste activated sludge to obtain class a biosolids. American Journal of Environmental Sciences, 6(6): 500–504

[3] Amoah I D, Reddy P, Seidu R, Stenström T A (2018). Concentration of soil-transmitted helminth eggs in sludge from South Africa and Senegal: A probabilistic estimation of infection risks associated with agricultural application. Journal of Environmental Management, 206: 1020–1027

[4] Amorós I, Moreno Y, Reyes M, Moreno-Mesonero L, Alonso J L (2016). Prevalence of Cryptosporidium oocysts and Giardia cysts in raw and treated sewage sludges. Environmental Technology, 37(22): 2898–2904

[5] Armstrong T W, Haas C N (2007). A quantitative microbial risk assessment model for Legionnaires’ disease: Animal model selection and dose-response modeling. Risk Analysis: An Official Publication of the Society for Risk Analysis, 27(6): 1581–1596

[6] Astals S, Venegas C, Peces M, Jofre J, Lucena F, Mata-Alvarez J (2012). Balancing hygienization and anaerobic digestion of raw sewage sludge. Water Research, 46(19): 6218–6227

[7] Bakheet B, Prodanovic V, Deletic A, McCarthy D (2020). Effective treatment of greywater via green wall biofiltration and electrochemical disinfection. Water Research, 185: 116228

[8] Balboa S, Mauricio-Iglesias M, Rodriguez S, Martínez-Lamas L, Vasallo F J, Regueiro B, Lema J M (2021). The fate of SARS-COV-2 in WWTPS points out the sludge line as a suitable spot for detection of COVID-19. Science of the Total Environment, 772: 145268

[9] Bardi M J, Oliaee M A (2021). Impacts of different operational temperatures and organic loads in anaerobic co-digestion of food waste and sewage sludge on the fate of SARS-CoV-2. Process Safety and Environmental Protection, 146: 464–472

[10] Bean C L, Hansen J J, Margolin A B, Balkin H, Batzer G, Widmer G (2007). Class B alkaline stabilization to achieve pathogen inactivation. International Journal of Environmental Research and Public Health, 4(1): 53–60

[11] Benito M, Menacho C, Chueca P, Ormad M P, Goñi P (2020). Seeking the reuse of effluents and sludge from conventional wastewater treatment plants: Analysis of the presence of intestinal protozoa and nematode eggs. Journal of Environmental Management, 261: 110268

[12] Bibby K, Peccia J (2013). Identification of viral pathogen diversity in sewage sludge by metagenome analysis. Environmental Science & Technology, 47(4): 1945–1951

[13] Boehm A B, Graham K E, Jennings W C (2018). Can we swim yet? Systematic review, meta-analysis, and risk assessment of aging sewage in surface waters. Environmental Science & Technology, 52(17): 9634–9645

[14] Borrely S I, Cruz A C, Del Mastro N L, Sampa M H O, Somessari E S (1998). Radiation processing of sewage and sludge: A review. Progress in Nuclear Energy, 33(1-2): 3–21

[15] Brooks J P, McLaughlin M R, Gerba C P, Pepper I L (2012). Land application of manure and Class B biosolids: An occupational and public quantitative microbial risk assessment. Journal of Environmental Quality, 41(6): 2009–2023

[16] Brooks J P, Tanner B D, Gerba C P, Haas C N, Pepper I L (2005). Estimation of bioaerosol risk of infection to residents adjacent to a land applied biosolids site using an empirically derived transport model. Journal of Applied Microbiology, 98(2): 397–405

[17] Buzzini A P, Patrizzi L J, Motheo A J, Pires E C (2007). Preliminary evaluation of the electrochemical and chemical coagulation processes in the post-treatment of effluent from an upflow anaerobic sludge blanket (UASB) reactor. Journal of Environmental Management, 85(4): 847–857

[18] Cai L, Zhang T (2013). Detecting human bacterial pathogens in wastewater treatment plants by a high-throughput shotgun sequencing technique. Environmental Science & Technology, 47(10): 5433–5441

[19] Calero-Cáceres W, Melgarejo A, Colomer-Lluch M, Stoll C, Lucena F, Jofre J, Muniesa M (2014). Sludge as a potential important source of antibiotic resistance genes in both the bacterial and bacteriophage fractions. Environmental Science & Technology, 48(13): 7602–7611

[20] Capizzi-Banas S, Deloge M, Remy M, Schwartzbrod J (2004). Liming as an advanced treatment for sludge sanitisation: Helminth eggs elimination: Ascaris eggs as model. Water Research, 38(14–15): 3251–3258

[21] Carraturo F, Del Giudice C, Morelli M, Cerullo V, Libralato G, Galdiero E, Guida M (2020). Persistence of SARS-CoV-2 in the environment and COVID-19 transmission risk from environmental matrices and surfaces. Environmental Pollution, 265(Pt B): 115010

[22] Chen J L, Ortiz R, Steele T W J, Stuckey D C (2014). Toxicants inhibiting anaerobic digestion: A review. Biotechnology Advances, 32(8): 1523–1534

[23] Chen Y H, Yan C, Yang Y F, Ma J X (2021). Quantitative microbial risk assessment and sensitivity analysis for workers exposed to pathogenic bacterial bioaerosols under various aeration modes in two wastewater treatment plants. Science of the Total Environment, 755(Pt 2): 142615

[24] Chetochine A S, Brusseau M L, Gerba C P, Pepper I L (2006). Leaching of phage from Class B biosolids and potential transport through soil. Applied and Environmental Microbiology, 72(1): 665–671

[25] Cheunbarn T, Pagilla K R (2000). Anaerobic thermophilic/mesophilic dual-stage sludge treatment. Journal of Environmental Engineering, 126(9): 796–801

[26] Chmielewski A G, Han B (2016). Electron Beam Technology for Environmental Pollution Control. Topics in Current Chemistry (Cham), 374(5): 68

[27] Claesson M J, Wang Q, O’Sullivan O, Greene-Diniz R, Cole J R, Ross R P, O’Toole P W (2010). Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Research, 38(22): e200

[28] Coelho N M G, Droste R L, Kennedy K J (2011). Evaluation of continuous mesophilic, thermophilic and temperature phased anaerobic digestion of microwaved activated sludge. Water Research, 45(9): 2822–2834

[29] Cosgun S, Semerci N (2019). Combined and individual applications of ozonation and microwave treatment for waste activated sludge solubilization and nutrient release. Journal of Environmental Management, 241: 76–83

[30] Cui X, Quicksall A N, Blake A B, Talley J W (2013). Electrochemical disinfection of Escherichia coli in the presence and absence of primary sludge particulates. Water Research, 47(13): 4383–4390

[31] Dai X, Li X, Yang W, Dai L, Dong B (2020). Virus in sewage sludge from wastewater treatment plant: Occurrence and potential risk during sludge treatment and disposal. Water & Wastewater Engineering, 46(3): 60–73 (in Chinese)

[32] Dauknys R, Mažeikienė A, Paliulis D (2020). Effect of ultrasound and high voltage disintegration on sludge digestion process. Journal of Environmental Management, 270: 110833

[33] Deng W, Su Y, Yu W (2013). Theoretical calculation of heat transfer coefficient when sludge drying in a nara-type paddle dryer using different heat carriers. Procedia Environmental Sciences, 18: 709–715

[34] Diehl D L, LaPara T M (2010). Effect of temperature on the fate of genes encoding tetracycline resistance and the integrase of class 1 integrons within anaerobic and aerobic digesters treating municipal wastewater solids. Environmental Science & Technology, 44(23): 9128–9133

[35] Drogui P, Bureau M A, Mercier G, Blais J F (2013). Effectiveness of electrooxidation process for stabilizing and conditioning of urban and industrial wastewater sludge. Water Environment Research: A Research Publication of the Water Environment Federation, 85(1): 35–43

[36] Eamens G J, Waldron A M, Nicholls P J (2006). Survival of pathogenic and indicator bacteria in biosolids applied to agricultural land. Australian Journal of Soil Research, 44(7): 647–659

[37] Eisenberg J N S, Moore K, Soller J A, Eisenberg D, Colford J M Jr (2008). Microbial risk assessment framework for exposure to amended sludge projects. Environmental Health Perspectives, 116(6): 727–733

[38] Elliott J G, Taylor-Edmonds L, Andrews R C (2019). Quantitative microbial risk assessments for drinking water facilities: Evaluation of a range of treatment strategies. Environmental Science. Water Research & Technology, 5(11): 1943–1955

[39] Elmerdahl Olsen J, Errebo Larsen H (1987). Bacterial decimation times in anaerobic digestions of animal slurries. Biological Wastes, 21(3): 153–168

[40] Elving J, Ottoson J R, Vinnerås B, Albihn A (2010). Growth potential of faecal bacteria in simulated psychrophilic/mesophilic zones during composting of organic waste. Journal of Applied Microbiology, 108(6): 1974–1981

[41] Espinosa M F, Sancho A N, Mendoza L M, Mota C R, Verbyla M E (2020). Systematic review and meta-analysis of time-temperature pathogen inactivation. International Journal of Hygiene and Environmental Health, 230: 113595

[42] Ferreira L C, Castro-Alférez M, Nahim-Granados S, Polo-López M I, Lucas M S, Li Puma G, Fernández-Ibáñez P (2020). Inactivation of water pathogens with solar photo-activated persulfate oxidation. Chemical Engineering Journal, 381: 122275

[43] Fidjeland J, Nordin A, Pecson B M, Nelson K L, Vinnerås B (2015). Modeling the inactivation of ascaris eggs as a function of ammonia concentration and temperature. Water Research, 83: 153–160

[44] Foladori P, Cutrupi F, Segata N, Manara S, Pinto F, Malpei F, Bruni L, La Rosa G (2020). SARS-CoV-2 from faeces to wastewater treatment: What do we know? A review. Science of the Total Environment, 743: 140444

[45] Font R, Gomez-Rico M F, Fullana A (2011). Skin effect in the heat and mass transfer model for sewage sludge drying. Separation and Purification Technology, 77(1): 146–161

[46] Forbis-Stokes A A, O’Meara P F, Mugo W, Simiyu G M, Deshusses M A (2016). On-Site Fecal Sludge Treatment with the Anaerobic Digestion Pasteurization Latrine. Environmental Engineering Science, 33(11): 898–906

[47] Forster-Carneiro T, Riau V, Pérez M (2010). Mesophilic anaerobic digestion of sewage sludge to obtain class B biosolids: Microbiological methods development. Biomass and Bioenergy, 34(12): 1805–1812

[48] Gale P (2003). Using event trees to quantify pathogen levels on root crops from land application of treated sewage sludge. Journal of Applied Microbiology, 94(1): 35–47

[49] Gale P (2005). Land application of treated sewage sludge: Quantifying pathogen risks from consumption of crops. Journal of Applied Microbiology, 98(2): 380–396

[50] Gantzer C, Gaspard P, Galvez L, Huyard A, Dumouthier N, Schwartzbrod J (2001). Monitoring of bacterial and parasitological contamination during various treatment of sludge. Water Research, 35(16): 3763–3770

[51] Gaviria-Figueroa A, Preisner E C, Hoque S, Feigley C E, Norman R S (2019). Emission and dispersal of antibiotic resistance genes through bioaerosols generated during the treatment of municipal sewage. Science of the Total Environment, 686: 402–412

[52] Ge D, Dong Y, Zhang W, Yuan H, Zhu N (2020). A novel Fe²⁺/persulfate/tannic acid process with strengthened efficacy on enhancing waste activated sludge dewaterability and mechanism insight. Science of the Total Environment, 733: 139146

[53] Gil A, Siles J A, Martín M A, Chica A F, Estévez-Pastor F S, Toro-Baptista E (2018). Effect of microwave pretreatment on semi-continuous anaerobic digestion of sewage sludge. Renewable Energy, 115: 917–925

[54] Goberna M, Simón P, Hernández M T, García C (2018). Prokaryotic communities and potential pathogens in sewage sludge: Response to wastewaster origin, loading rate and treatment technology. Science of the Total Environment, 615: 360–368

[55] Gomes L A, Santos A F, Pinheiro C T, Góis J C, Quina M J (2020). Screening of waste materials as adjuvants for drying sewage sludge based on environmental, technical and economic criteria. Journal of Cleaner Production, 259: 120927

[56] Graff J, Ticehurst J, Flehmig B (1993). Detection of hepatitis A virus in sewage sludge by antigen capture polymerase chain reaction. Applied and Environmental Microbiology, 59(10): 3165–3170

[57] Grübel K, Suschka J (2015). Hybrid alkali-hydrodynamic disintegration of waste-activated sludge before two-stage anaerobic digestion process. Environmental Science and Pollution Research International, 22(10): 7258–7270

[58] Guajardo-Leiva S, Chnaiderman J, Gaggero A, Díez B (2020). Metagenomic Insights into the sewage RNA virosphere of a large city. Viruses, 12(9): 1050

[59] Hait S, Tare V (2011). Optimizing vermistabilization of waste activated sludge using vermicompost as bulking material. Waste Management (New York, N.Y.), 31(3): 502–511

[60] Hamilton K A, Haas C N (2016). Critical review of mathematical approaches for quantitative microbial risk assessment (QMRA) of Legionella in engineered water systems: research gaps and a new framework. Environmental Science. Water Research & Technology, 2(4): 599–613

[61] Hamilton K A, Hamilton M T, Johnson W, Jjemba P, Bukhari Z, LeChevallier M, Haas C N, Gurian P L (2019). Risk-based critical concentrations of Legionella pneumophila for indoor residential water uses. Environmental Science & Technology, 53(8): 4528–4541

[62] Han Y P, Li L, Wang Y, Ma J W, Li P Y, Han C, Liu J X (2021). Composition, dispersion, and health risks of bioaerosols in wastewater treatment plants: A review. Frontiers of Environmental Science & Engineering, 15(3): 16

[63] Hansen J J, Warden P S, Margolin A B (2007). Inactivation of adenovirus type 5, rotavirus Wa and male specific coliphage (MS2) in biosolids by lime stabilization. International Journal of Environmental Research and Public Health, 4(1): 61–67

[64] Hong S M, Park J K, Lee Y O (2004). Mechanisms of microwave irradiation involved in the destruction of fecal coliforms from biosolids. Water Research, 38(6): 1615–1625

[65] Hong S M, Park J K, Teeradej N, Lee Y O, Cho Y K, Park C H (2006). Pretreatment of sludge with microwaves for pathogen destruction and improved anaerobic digestion performance. Water Environment Research: A Research Publication of the Water Environment Federation, 78(1): 76–83

[66] Hu S, Zhao W, Hu J, Liu B, Wang D, Zhu Q, Yang J, Hou H (2021). Integration of electrochemical and calcium hypochlorite oxidation for simultaneous sludge deep dewatering, stabilization and phosphorus fixation. Science of the Total Environment, 750: 141408

[67] Hu Y, Wang F, Lv G, Chi Y (2019). Enhancing the biogas production of sludge anaerobic digestion by a combination of zero-valent iron foil and persulfate. Energy & Fuels, 33(8): 7436–7442

[68] Huang J, Elektorowicz M, Oleszkiewicz J A (2008). Dewatering and disinfection of aerobic and anaerobic sludge using an electrokinetic (EK) system. Water Science and Technology: A Journal of the International Association on Water Pollution Research, 57(2): 231–236

[69] Huang K, Mao Y, Zhao F, Zhang X X, Ju F, Ye L, Wang Y, Li B, Ren H, Zhang T (2018). Free-living bacteria and potential bacterial pathogens in sewage treatment plants. Applied Microbiology and Biotechnology, 102(5): 2455–2464

[70] Huang K, Xia H, Zhang Y, Li J, Cui G, Li F, Bai W, Jiang Y, Wu N (2020). Elimination of antibiotic resistance genes and human pathogenic bacteria by earthworms during vermicomposting of dewatered sludge by metagenomic analysis. Bioresource Technology, 297: 122451

[71] Inglis G D, McAllister T A, Larney F J, Topp E (2010). Prolonged survival of Campylobacter species in bovine manure compost. Applied and Environmental Microbiology, 76(4): 1110–1119

[72] Iranpour R, Cox H H J (2006). Recurrence of fecal coliforms and Salmonella species in biosolids following thermophilic anaerobic digestion. Water Environment Research: A Research Publication of the Water Environment Federation, 78(9): 1005–1012

[73] Iranpour R, Cox H H J (2007). Evaluation of thermophilic anaerobic digestion processes for full-scale Class A biosolids disinfection at Hyperion Treatment Plant. Biotechnology and Bioengineering, 97(1): 19–39

[74] Jafari M, Botte G G (2021). Electrochemical treatment of sewage sludge and pathogen inactivation. Journal of Applied Electrochemistry, 51(1): 119–130

[75] Jahne M A, Brinkman N E, Keely S P, Zimmerman B D, Wheaton E A, Garland J L (2020). Droplet digital PCR quantification of norovirus and adenovirus in decentralized wastewater and graywater collections: Implications for onsite reuse. Water Research, 169: 115213

[76] Jebri S, Hmaied F, Lucena F, Saavedra M E, Yahya M, Hamdi M (2014). A comparison of two extraction methods for the detection of Enteroviruses in raw sludge. Journal of Virological Methods, 200: 1–5

[77] Jin B, Niu J, Zhang J, Niu J, Zhou P, Dai J, Li N, Tao H, Ma Z, Zhang Z (2020). Response of extracellular polymeric substances and enzymatic activity to salinity for the waste activated sludge anaerobic fermentation process. Bioprocess and Biosystems Engineering, 43(4): 737–745

[78] Ju F, Lau F, Zhang T (2017). Linking Microbial Community, Environmental Variables, and Methanogenesis in Anaerobic Biogas Digesters of Chemically Enhanced Primary Treatment Sludge. Environmental Science & Technology, 51(7): 3982–3992

[79] 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 Research, 91: 1–10

[80] Jyoti A, Vajpayee P, Singh G, Patel C B, Gupta K C, Shanker R (2011). Identification of environmental reservoirs of nontyphoidal salmonellosis: Aptamer-assisted bioconcentration and subsequent detection of salmonella typhimurium by quantitative polymerase chain reaction. Environmental Science & Technology, 45(20): 8996–9002

[81] Kabrick R M, Jewell W J (1982). Fate of pathogens in thermophilic aerobic sludge digestion. Water Research, 16(6): 1051–1060

[82] Kearney T E, Larkin M J, Levett P N (1993). The effect of slurry storage and anaerobic digestion on survival of pathogenic bacteria. Journal of Applied Bacteriology, 74(1): 86–93

[83] Kelessidis A, Stasinakis A S (2012). Comparative study of the methods used for treatment and final disposal of sewage sludge in European countries. Waste Management (New York, N.Y.), 32(6): 1186–1195

[84] Kennedy N A, Walker A W, Berry S H, Duncan S H, Farquarson F M, Louis P, Thomson J M, Satsangi J, Flint H J, Parkhill J, Lees C W, Hold G L, and the UK IBD Genetics Consortium (2014). The impact of different DNA extraction kits and laboratories upon the assessment of human gut microbiota composition by 16S rRNA gene sequencing. PLoS One, 9(2): e88982

[85] Khwairakpam M, Bhargava R (2009). Vermitechnology for sewage sludge recycling. Journal of Hazardous Materials, 161(2-3): 948–954

[86] Kim T H, Lee M, Park C (2011). Gamma ray irradiation for sludge solubilization and biological nitrogen removal. Radiation Physics and Chemistry, 80(12): 1386–1390

[87] Kong F E, Deighton M A, Thurbon N A, Smith S R, Rouch D A (2018). Cryptosporidium parvum decay during air drying and stockpiling of mesophilic anaerobically digested sewage sludge in a simulation experiment and oocyst counts in sludge collected from operational treatment lagoons in Victoria, Australia. Journal of Water and Health, 16(3): 435–448

[88] Lagier J C, Armougom F, Million M, Hugon P, Pagnier I, Robert C, Bittar F, Fournous G, Gimenez G, Maraninchi M, Trape J F, Koonin E V, La Scola B, Raoult D (2012). Microbial culturomics: paradigm shift in the human gut microbiome study. Clinical Microbiology and Infection: The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases, 18(12): 1185–1193

[89] Lammerding A M (2006). Modeling and risk assessment for Salmonella in meat and poultry. Journal of AOAC International, 89(2): 543–552

[90] Lau C H F, Li B, Zhang T, Tien Y C, Scott A, Murray R, Sabourin L, Lapen D R, Duenk P, Topp E (2017). Impact of pre-application treatment on municipal sludge composition, soil dynamics of antibiotic resistance genes, and abundance of antibiotic-resistance genes on vegetables at harvest. Science of the Total Environment, 587-588: 214–222

[91] Lei Q, Zheng J, Ma J, Wang X, Wu Z, Wang Z (2020). Simultaneous solid-liquid separation and wastewater disinfection using an electrochemical dynamic membrane filtration system. Environmental Research, 180: 108861

[92] Levantesi C, Beimfohr C, Blanch A R, Carducci A, Gianico A, Lucena F, Tomei M C, Mininni G (2015). Hygienization performances of innovative sludge treatment solutions to assure safe land spreading. Environmental Science and Pollution Research International, 22(10): 7237–7247

[93] Lewis D L, Gattie D K (2002). Pathogen risks from applying sewage sludge to land. Environmental Science & Technology, 36(13): 286A–293A

[94] Li B, Ju F, Cai L, Zhang T (2015). Profile and fate of bacterial pathogens in sewage treatment plants revealed by high-throughput metagenomic approach. Environmental Science & Technology, 49(17): 10492–10502

[95] Li D C, Gao J F, Zhang S J, Gao Y Q, Sun L X (2020a). Emergence and spread patterns of antibiotic resistance genes during two different aerobic granular sludge cultivation processes. Environment International, 137: 105540

[96] Li J, Zhou L T, Zhang X Y, Xu C J, Dong L M, Yao M S (2016a). Bioaerosol emissions and detection of airborne antibiotic resistance genes from a wastewater treatment plant. Atmospheric Environment, 124: 404–412

[97] Li M, Yang Y, Lu Y, Zhang D, Liu Y, Cui X, Yang L, Liu R, Liu J, Li G, Qu J (2020b). Natural host-environmental media-human: A new potential pathway of COVID-19 outbreak. Engineering (Beijing, China), 6(10): 1085–1098

[98] Li X, Li Y, Hong L (2016b). A novel self-assembling DNA nano chip for rapid detection of human Papillomavirus genes. PLoS One, 11(10): e0162975

[99] Liao H, Lu X, Rensing C, Friman V P, Geisen S, Chen Z, Yu Z, Wei Z, Zhou S, Zhu Y (2018). Hyperthermophilic composting accelerates the removal of antibiotic resistance genes and mobile genetic elements in sewage sludge. Environmental Science & Technology, 52(1): 266–276

[100] Liu S, Zhu N, Li L Y (2011). The one-stage autothermal thermophilic aerobic digestion for sewage sludge treatment. Chemical Engineering Journal, 174(2-3): 564–570

[101] Lizasoain A, Tort L F L, García M, Gillman L, Alberti A, Leite J P G, Miagostovich M P, Pou S A, Cagiao A, Razsap A, Huertas J, Berois M, Victoria M, Colina R (2018). Human enteric viruses in a wastewater treatment plant: Evaluation of activated sludge combined with UV disinfection process reveals different removal performances for viruses with different features. Letters in Applied Microbiology, 66(3): 215–221

[102] Lloret E, Pastor L, Martínez-Medina A, Blaya J, Pascual J A (2012). Evaluation of the removal of pathogens included in the Proposal for a European Directive on spreading of sludge on land during autothermal thermophilic aerobic digestion (ATAD). Chemical Engineering Journal, 198–199: 171–179

[103] Lloret E, Pastor L, Pradas P, Pascual J A (2013). Semi full-scale thermophilic anaerobic digestion (TAnD) for advanced treatment of sewage sludge: Stabilization process and pathogen reduction. Chemical Engineering Journal, 232: 42–50

[104] López A, Rodríguez-Chueca J, Mosteo R, Gómez J, Ormad M P (2020). Microbiological quality of sewage sludge after digestion treatment: A pilot scale case of study. Journal of Cleaner Production, 254: 120101

[105] Lu F, Hu T Y, Wei S Y, Shao L M, He P J(2021). Bioaerosolization behavior along sewage sludge biostabilization. Frontiers of Environmental Science & Engineering, 15(3): 45

[106] Lu X, Zhang X X, Wang Z, Huang K, Wang Y, Liang W, Tan Y, Liu B, Tang J (2015). Bacterial pathogens and community composition in advanced sewage treatment systems revealed by metagenomics analysis based on high-throughput sequencing. PLoS One, 10(5): e0125549

[107] Lung A J, Lin C M, Kim J M, Marshall M R, Nordstedt R, Thompson N P, Wei C I (2001). Destruction of Escherichia coli O157:H7 and Salmonella enteritidis in cow manure composting. Journal of Food Protection, 64(9): 1309–1314

[108] Luukkonen T, Prokkola H, Pehkonen S O (2020). Peracetic acid for conditioning of municipal wastewater sludge: Hygienization, odor control, and fertilizing properties. Waste Management (New York, N.Y.), 102: 371–379

[109] Lv B, Xing M, Yang J (2018). Exploring the effects of earthworms on bacterial profiles during vermicomposting process of sewage sludge and cattle dung with high-throughput sequencing. Environmental Science and Pollution Research International, 25(13): 12528–12537

[110] Magri M E, Fidjeland J, Jönsson H, Albihn A, Vinnerås B (2015). Inactivation of adenovirus, reovirus and bacteriophages in fecal sludge by pH and ammonia. Science of the Total Environment, 520: 213–221

[111] Major N, Schierstaedt J, Jechalke S, Nesme J, Ban S G, Černe M, Sørensen S J, Ban D, Schikora A (2020). Composted Sewage Sludge Influences the Microbiome and Persistence of Human Pathogens in Soil. Microorganisms, 8(7): 1020

[112] Mandilara G, Mavridou A, Lambiri M, Vatopoulos A, Rigas F (2006). The use of bacteriophages for monitoring the microbiological quality of sewage sludge. Environmental Technology, 27(4): 367–375

[113] Maqbool T, Cho J, Hur J (2019). Improved dewaterability of anaerobically digested sludge and compositional changes in extracellular polymeric substances by indigenous persulfate activation. Science of the Total Environment, 674: 96–104

[114] Martín-Díaz J, Lucena F, Blanch A R, Jofre J (2020). Review: Indicator bacteriophages in sludge, biosolids, sediments and soils. Environmental Research, 182: 109133

[115] Mawioo P M, Garcia H A, Hooijmans C M, Velkushanova K, Simonič M, Mijatović I, Brdjanovic D (2017). A pilot-scale microwave technology for sludge sanitization and drying. Science of the Total Environment, 601-602: 1437–1448

[116] Mehta C M, Palni U, Franke-Whittle I H, Sharma A K (2014). Compost: its role, mechanism and impact on reducing soil-borne plant diseases. Waste Management (New York, N.Y.), 34(3): 607–622

[117] Mignotte-Cadiergues B, Gantzer C, Schwartzbrod L (2002). Evaluation of bacteriophages during the treatment of sludge. Water Science and Technology: A Journal of the International Association on Water Pollution Research, 46(10): 189–194

[118] Millner P D, Powers K E, Enkiri N K, Burge W D (1987). Microbially mediated growth suppression and death of salmonella in composted sewage sludge. Microbial Ecology, 14(3): 255–265

[119] Min Jang H, Choi S, Shin J, Kan E, Mo Kim Y (2019). Additional reduction of antibiotic resistance genes and human bacterial pathogens via thermophilic aerobic digestion of anaerobically digested sludge. Bioresource Technology, 273: 259–268

[120] Mocé-Llivina L, Muniesa M, Pimenta-Vale H, Lucena F, Jofre J (2003). Survival of bacterial indicator species and bacteriophages after thermal treatment of sludge and sewage. Applied and Environmental Microbiology, 69(3): 1452–1456

[121] Moletta-Denat M, Bru-Adan V, Delgenes J P, Hamelin J, Wéry N, Godon J J (2010). Selective microbial aerosolization in biogas demonstrated by quantitative PCR. Bioresource Technology, 101(19): 7252–7257

[122] Mondal T, Rouch D A, Thurbon N, Smith S R, Deighton M A (2015). Factors affecting decay of Salmonella Birkenhead and coliphage MS2 during mesophilic anaerobic digestion and air drying of sewage sludge. Journal of Water and Health, 13(2): 459–472

[123] Monpoeho S, Maul A, Bonnin C, Patria L, Ranarijaona S, Billaudel S, Ferré V (2004). Clearance of human-pathogenic viruses from sludge: study of four stabilization processes by real-time reverse transcription-PCR and cell culture. Applied and Environmental Microbiology, 70(9): 5434–5440

[124] Monroy F, Aira M, Domínguez J (2009). Reduction of total coliform numbers during vermicomposting is caused by short-term direct effects of earthworms on microorganisms and depends on the dose of application of pig slurry. Science of the Total Environment, 407(20): 5411–5416

[125] Mosquera-Losada M R, Rigueiro-Rodríguez A, Ferreiro-Domínguez N (2012). Residual effects of lime and sewage sludge inputs on soil fertility and tree and pasture production in a Pinus radiata D. Don silvopastoral system established in a very acidic soil. Agriculture, Ecosystems & Environment, 161: 165–173

[126] Naidoo D, Appleton C C, Archer C E, Foutch G L (2019). The inactivation of Ascaris suum eggs by short exposure to high temperatures. Journal of Water, Sanitation, and Hygiene for Development : a Journal of the International Water Association, 9(1): 19–27

[127] Navab Daneshmand T, Beton R, Hill R J, Gehr R, Frigon D (2012). Inactivation mechanisms of bacterial pathogen indicators during electro-dewatering of activated sludge biosolids. Water Research, 46(13): 3999–4008

[128] Navarro I, Jiménez B, Lucario S, Cifuentes E (2009). Application of Helminth ova infection dose curve to estimate the risks associated with biosolid application on soil. Journal of Water and Health, 7(1): 31–44

[129] Orzi V, Scaglia B, Lonati S, Riva C, Boccasile G, Alborali G L, Adani F (2015). The role of biological processes in reducing both odor impact and pathogen content during mesophilic anaerobic digestion. Science of the Total Environment, 526: 116–126

[130] Paez-Rubio T, Ramarui A, Sommer J, Xin H, Anderson J, Peccia J (2007). Emission rates and characterization of aerosols produced during the spreading of dewatered class B biosolids. Environmental Science & Technology, 41(10): 3537–3544

[131] Pandey P K, Soupir M L (2011). Escherichia coli inactivation kinetics in anaerobic digestion of dairy manure under moderate, mesophilic and thermophilic temperatures. AMB Express, 1(1): 18

[132] Pecson B M, Barrios J A, Jiménez B E, Nelson K L (2007). The effects of temperature, pH, and ammonia concentration on the inactivation of Ascaris eggs in sewage sludge. Water Research, 41(13): 2893–2902

[133] Pietronave S, Fracchia L, Rinaldi M, Martinotti M G (2004). Influence of biotic and abiotic factors on human pathogens in a finished compost. Water Research, 38(8): 1963–1970

[134] Plachá I, Venglovský J, Maková Z, Martinéz J (2008). The elimination of Salmonella typhimurium in sewage sludge by aerobic mesophilic stabilization and lime hydrated stabilization. Bioresource Technology, 99(10): 4269–4274

[135] Prado T, Gaspar A M C, Miagostovich M P (2014). Detection of enteric viruses in activated sludge by feasible concentration methods. Brazilian Journal of Microbiology, 45(1): 343–349

[136] Pritchard D L, Penney N, McLaughlin M J, Rigby H, Schwarz K (2010). Land application of sewage sludge (biosolids) in Australia: Risks to the environment and food crops. Water Science and Technology: A Journal of the International Association on Water Pollution Research, 62(1): 48–57

[137] Quince C, Walker A W, Simpson J T, Loman N J, Segata N (2017). Shotgun metagenomics, from sampling to analysis. Nature Biotechnology, 35(9): 833–844

[138] Rahube T O, Marti R, Scott A, Tien Y C, Murray R, Sabourin L, Zhang Y, Duenk P, Lapen D R, Topp E (2014). Impact of fertilizing with raw or anaerobically digested sewage sludge on the abundance of antibiotic-resistant coliforms, antibiotic resistance genes, and pathogenic bacteria in soil and on vegetables at harvest. Applied and Environmental Microbiology, 80(22): 6898–6907

[139] Rajagopal R, Massé D I, Singh G (2013). A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresource Technology, 143: 632–641

[140] Ranković B, Sagatova A, Vujcic I, Masic S, Veljovic D, Pavicevic V, Kamberovic Z (2020). Utilization of gamma and e-beam irradiation in the treatment of waste sludge from a drinking water treatment plant. Radiation Physics and Chemistry, 177: 109177

[141] 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

[142] Robledo-Mahón , Gómez-Silván C, Andersen G L, Calvo C, Aranda E (2020). Assessment of bacterial and fungal communities in a full-scale thermophilic sewage sludge composting pile under a semipermeable cover. Bioresource Technology, 298: 122550

[143] Robledo-Mahón T, Silva-Castro G A, Kuhar U, Jamnikar-Ciglenečki U, Barlič-Maganja D, Aranda E, Calvo C (2019). Effect of composting under semipermeable film on the sewage sludge virome. Microbial Ecology, 78(4): 895–903

[144] Romdhana M H, Lecomte D, Ladevie B, Sablayrolles C (2009). Monitoring of pathogenic microorganisms contamination during heat drying process of sewage sludge. Process Safety and Environmental Protection, 87(6): 377–386

[145] Rumky J, Visigalli S, Turolla A, Gelmi E, Necibi C, Gronchi P, Sillanpää M, Canziani R (2020). Electro-dewatering treatment of sludge: Assessment of the influence on relevant indicators for disposal in agriculture. Journal of Environmental Management, 268: 110689

[146] Sado K, Ayusawa D, Enomoto A, Suganuma T, Oshimura M, Sato K, Koyama H (2001). Identification of a mutated DNA ligase IV gene in the X-ray-hypersensitive mutant SX10 of mouse FM3A cells. Journal of Biological Chemistry, 276(13): 9742–9748

[147] Sahlström L (2003). A review of survival of pathogenic bacteria in organic waste used in biogas plants. Bioresource Technology, 87(2): 161–166

[148] Sano D, Fukushi K, Yoshida Y, Omura T (2003). Detection of enteric viruses in municipal sewage sludge by a combination of the enzymatic virus elution method and RT-PCR. Water Research, 37(14): 3490–3498

[149] Santos A F, Santos C P, Matos A M, Cardoso O, Quina M J (2020). Effect of thermal drying and chemical treatments with wastes on microbiological contamination indicators in sewage sludge. Microorganisms, 8(3): 376

[150] Schlosser O, Huyard A, Cartnick K, Yañez A, Catalán V, Do Quang Z (2009). Bioaerosol in composting facilities: Occupational health risk assessment. Water Environment Research: A Research Publication of the Water Environment Federation, 81(9): 866–877

[151] Schlosser O, Robert S, Debeaupuis C, Huyard A (2018). Inhalable dust as a marker of exposure to airborne biological agents in composting facilities. Waste Management (New York, N.Y.), 81: 78–87

[152] Schöniger-Hekele M, Petermann D, Weber B, Müller C (2007). Tropheryma whipplei in the environment: survey of sewage plant influxes and sewage plant workers. Applied and Environmental Microbiology, 73(6): 2033–2035

[153] Sen B, Chandra T S (2009). Do earthworms affect dynamics of functional response and genetic structure of microbial community in a lab-scale composting system? Bioresource Technology, 100(2): 804–811

[154] Shannon K E, Lee D Y, Trevors J T, Beaudette L A (2007). Application of real-time quantitative PCR for the detection of selected bacterial pathogens during municipal wastewater treatment. Science of the Total Environment, 382(1): 121–129

[155] Sidhu J, Gibbs R A, Ho G E, Unkovich I (2001). The role of indigenous microorganisms in suppression of Salmonella regrowth in composted biosolids. Water Research, 35(4): 913–920

[156] Simmons F J, Xagoraraki I (2011). Release of infectious human enteric viruses by full-scale wastewater utilities. Water Research, 45(12): 3590–3598

[157] Soobhany N, Mohee R, Garg V K (2017). Inactivation of bacterial pathogenic load in compost against vermicompost of organic solid waste aiming to achieve sanitation goals: A review. Waste Management (New York, N.Y.), 64: 51–62

[158] Soueidan H, Schmitt L A, Candresse T, Nikolski M (2015). Finding and identifying the viral needle in the metagenomic haystack: trends and challenges. Frontiers in Microbiology, 5: 739

[159] Su J Q, Wei B, Ou-Yang W Y, Huang F Y, Zhao Y, Xu H J, Zhu Y G (2015). Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environmental Science & Technology, 49(12): 7356–7363

[160] Sutherland K P, Porter J W, Turner J W, Thomas B J, Looney E E, Luna T P, Meyers M K, Futch J C, Lipp E K (2010). Human sewage identified as likely source of white pox disease of the threatened Caribbean elkhorn coral, Acropora palmata. Environmental Microbiology, 12(5): 1122–1131

[161] Swati A, Hait S (2018). A Comprehensive Review of the Fate of Pathogens during Vermicomposting of Organic Wastes. Journal of Environmental Quality, 47(1): 16–29

[162] Tanner B D, Brooks J P, Gerba C P, Haas C N, Josephson K L, Pepper I L (2008). Estimated occupational risk from bioaerosols generated during land application of class B biosolids. Journal of Environmental Quality, 37(6): 2311–2321

[163] Tong J, Fang P, Zhang J, Wei Y, Su Y, Zhang Y (2019). Microbial community evolution and fate of antibiotic resistance genes during sludge treatment in two full-scale anaerobic digestion plants with thermal hydrolysis pretreatment. Bioresource Technology, 288: 121575

[164] Tong M, Liu F, Dong Q, Ma Z, Liu W (2020). Magnetic Fe₃O₄-deposited flower-like MoS₂ nanocomposites for the Fenton-like Escherichia coli disinfection and diclofenac degradation. Journal of Hazardous Materials, 385: 121604

[165] Traub F, Spillmann S K, Wyler R (1986). Method for determining virus inactivation during sludge treatment processes. Applied and Environmental Microbiology, 52(3): 498–503

[166] Tsitsifli S, Tsoukalas D S (2021). Water Safety Plans and HACCP implementation in water utilities around the world: benefits, drawbacks and critical success factors. Environmental Science and Pollution Research International, 28(15): 18837–18849

[167] Uma Rani R, Adish Kumar S, Kaliappan S, Yeom I, Rajesh Banu J (2013). Impacts of microwave pretreatments on the semi-continuous anaerobic digestion of dairy waste activated sludge. Waste Management (New York, N.Y.), 33(5): 1119–1127

[168] USEPA (1994). Land application of sewage sludge: A guide for land appliers on the requirements of the federal standard for the use or disposal of sewage sludge, 40 CFR Part 503. USEPA, Washington, DC. EPA/831-B-93-002b.

[169] Valderrama C, Granados R, Cortina J L (2013). Stabilisation of dewatered domestic sewage sludge by lime addition as raw material for the cement industry: Understanding process and reactor performance. Chemical Engineering Journal, 232: 458–467

[170] Van Abel N, Schoen M E, Kissel J C, Meschke J S (2017). Comparison of risk predicted by multiple norovirus dose-response models and implications for quantitative microbial risk Assessment. Risk Analysis: An Official Publication of the Society for Risk Analysis, 37(2): 245–264

[171] Venieri D, Karapa A, Panagiotopoulou M, Gounaki I (2020). Application of activated persulfate for the inactivation of fecal bacterial indicators in water. Journal of Environmental Management, 261: 110223

[172] Viau E, Bibby K, Paez-Rubio T, Peccia J (2011). Toward a consensus view on the infectious risks associated with land application of sewage sludge. Environmental Science & Technology, 45(13): 5459–5469

[173] Viau E, Peccia J (2009). Survey of wastewater indicators and human pathogen genomes in biosolids produced by Class A and Class B stabilization treatments. Applied and Environmental Microbiology, 75(1): 164–174

[174] Walker A W, Martin J C, Scott P, Parkhill J, Flint H J, Scott K P (2015). 16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice. Microbiome, 3(1): 26

[175] Wang J, Wang J (2007). Application of radiation technology to sewage sludge processing: A review. Journal of Hazardous Materials, 143(1–2): 2–7

[176] Wang M, Chen H, Liu S, Xiao L (2021). Removal of pathogen and antibiotic resistance genes from waste activated sludge by different pre-treatment approaches. Science of the Total Environment, 763: 143014

[177] Wang M L, Li R Y, Zhao Q (2019). Distribution and removal of antibiotic resistance genes during anaerobic sludge digestion with alkaline, thermal hydrolysis and ultrasonic pretreatments. Frontiers of Environmental Science & Engineering, 13(3): 43

[178] Wang W, Wang H, Li G, Wong P K, An T (2020). Visible light activation of persulfate by magnetic hydrochar for bacterial inactivation: Efficiency, recyclability and mechanisms. Water Research, 176: 115746

[179] Ward R L, Ashley C S (1978). Heat inactivation of enteric viruses in dewatered wastewater sludge. Applied and Environmental Microbiology, 36(6): 898–905

[180] Watanabe T, Sano D, Omura T (2002). Risk evaluation for pathogenic bacteria and viruses in sewage sludge compost. Water Science and Technology: A Journal of the International Association on Water Pollution Research, 46(11–12): 325–330

[181] Watcharasukarn M, Kaparaju P, Steyer J P, Krogfelt K A, Angelidaki I (2009). Screening Escherichia coli, Enterococcus faecalis, and Clostridium perfringens as indicator organisms in evaluating pathogen-reducing capacity in biogas plants. Microbial Ecology, 58(2): 221–230

[182] Wéry N, Lhoutellier C, Ducray F, Delgenès J P, Godon J J (2008). Behaviour of pathogenic and indicator bacteria during urban wastewater treatment and sludge composting, as revealed by quantitative PCR. Water Research, 42(1-2): 53–62

[183] Wichuk K M, Mccartney D (2007). A review of the effectiveness of current time-temperature regulations on pathogen inactivation during composting. Journal of Environmental Engineering and Science, 6(5): 573–586

[184] Wong J W C, Selvam A (2009). Reduction of indicator and pathogenic microorganisms in pig manure through fly ash and lime addition during alkaline stabilization. Journal of Hazardous Materials, 169(1-3): 882–889

[185] Wong K, Onan B M, Xagoraraki I (2010). Quantification of enteric viruses, pathogen indicators, and Salmonella bacteria in Class B anaerobically digested biosolids by culture and molecular methods. Applied and Environmental Microbiology, 76(19): 6441–6448

[186] Wu Y, Jiang Y, Ke G, Liu Y (2017). Effect of gamma-ray irradiation on the dewaterability of waste activated sludge. Radiation Physics and Chemistry, 130: 164–170

[187] Xu P, Zhang C, Mou X, Wang X C (2020). Bioaerosol in a typical municipal wastewater treatment plant: concentration, size distribution, and health risk assessment. Water Science and Technology: A Journal of the International Association on Water Pollution Research, 82(8): 1547–1559

[188] Yan C, Wang R N, Zhao X Y (2021). Emission characteristics of bioaerosol and quantitative microbiological risk assessment for equipping individuals with various personal protective equipment in a WWTP. Chemosphere, 265: 129117

[189] Yang G, Zhang G, Wang H (2015). Current state of sludge production, management, treatment and disposal in China. Water Research, 78: 60–73

[190] Yang K, Li L, Wang Y, Xue S, Han Y, Liu J (2019). Airborne bacteria in a wastewater treatment plant: Emission characterization, source analysis and health risk assessment. Water Research, 149: 596–606

[191] Yang W, Cai C, Dai X (2020). The potential exposure and transmission risk of SARS-CoV-2 through sludge treatment and disposal. Resources, Conservation and Recycling, 162: 105043

[192] Ye L, Zhang T (2011). Pathogenic bacteria in sewage treatment plants as revealed by 454 pyrosequencing. Environmental Science & Technology, 45(17): 7173–7179

[193] Yenigün O, Demirel B (2013). Ammonia inhibition in anaerobic digestion: A review. Process Biochemistry, 48(5–6): 901–911

[194] Yin F B, Li Z F, Saino M, Dong H M (2017). Performance of alkaline pretreatment on pathogens inactivation and sludge solubilization. International Journal of Agricultural and Biological Engineering, 10(2): 216–223

[195] Yin Z, Hoffmann M, Jiang S (2018). Sludge disinfection using electrical thermal treatment: The role of ohmic heating. Science of the Total Environment, 615: 262–271

[196] Yu B, Zheng G D, Wang X D, Wang M, Chen T B (2019a). Biodegradation of triclosan and triclocarban in sewage sludge during composting under three ventilation strategies. Frontiers of Environmental Science & Engineering, 13(3): 41

[197] Yu D T, He J Z, Zhang L M, Han L L (2019b). Viral metagenomics analysis and eight novel viral genomes identified from the Dushanzi mud Volcanic soil in Xinjiang, China. Journal of Soils and Sediments, 19(1): 81–90

[198] Yu J, Xiao K, Yang J, Yu W, Pei K, Zhu Y, Wang J, Liang S, Hu J, Hou H, Liu B (2019c). Enhanced sludge dewaterability and pathogen inactivation by synergistic effects of zero-valent iron and ozonation. ACS Sustainable Chemistry & Engineering, 7(1): 324–331

[199] Yu R, Zhang S W, Chen Z K, Li C Y (2017). Isolation and application of predatory Bdellovibrio-and-like organisms for municipal waste sludge biolysis and dewaterability enhancement. Frontiers of Environmental Science & Engineering, 11(1): 10

[200] Yu W, Wen Q, Yang J, Xiao K, Zhu Y, Tao S, Lv Y, Liang S, Fan W, Zhu S, Liu B, Hou H, Hu J (2019d). Unraveling oxidation behaviors for intracellular and extracellular from different oxidants (HOCl vs. H₂O₂) catalyzed by ferrous iron in waste activated sludge dewatering. Water Research, 148: 60–69

[201] Yu Y, Chan W I, Liao P H, Lo K V (2010). Disinfection and solubilization of sewage sludge using the microwave enhanced advanced oxidation process. Journal of Hazardous Materials, 181(1-3): 1143–1147

[202] Zaleski K J, Josephson K L, Gerba C P, Pepper I L (2005). Potential regrowth and recolonization of salmonellae and indicators in biosolids and biosolid-amended soil. Applied and Environmental Microbiology, 71(7): 3701–3708

[203] Zaneti R N, Girardi V, Spilki F R, Mena K, Westphalen A P C, da Costa Colares E R, Pozzebon A G, Etchepare R G (2021). Quantitative microbial risk assessment of SARS-CoV-2 for workers in wastewater treatment plants. Science of the Total Environment, 754: 142163

[204] Zeng Q, Zan F, Hao T, Biswal B K, Lin S, van Loosdrecht M C M, Chen G (2019). Electrochemical pretreatment for stabilization of waste activated sludge: Simultaneously enhancing dewaterability, inactivating pathogens and mitigating hydrogen sulfide. Water Research, 166: 115035

[205] Zhang H, Xu L, Zhang Y F, Jiang M C (2016). The transformation of PAHs in the sewage sludge incineration treatment. Frontiers of Environmental Science & Engineering, 10(2): 336–340

[206] Zhang H, Zhang Z, Song J, Cai L, Yu Y, Fang H (2021). Foam shares antibiotic resistomes and bacterial pathogens with activated sludge in wastewater treatment plants. Journal of Hazardous Materials, 408: 124855

[207] Zhang L, Chen Y, Ma C, Liu L, Pan J, Li B, Wu X, Wang Q (2020). Improving heavy metals removal, dewaterability and pathogen removal of waste activated sludge using enhanced chemical leaching. Journal of Cleaner Production, 271: 122512

[208] Zhang T, Zhang M, Zhang X, Fang H H (2009). Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environmental Science & Technology, 43(10): 3455–3460

[209] Zhao Q, Liu Y (2019). Is anaerobic digestion a reliable barrier for deactivation of pathogens in biosludge? Science of the Total Environment, 668: 893–902

[210] Zimek Z (2020). Economical evaluation of radiation processing with high-intensity X-rays. Nukleonika, 65(3): 167–172

[211] Zou X, Tang G, Zhao X, Huang Y, Chen T, Lei M, Chen W, Yang L, Zhu W, Zhuang L, Yang J, Feng Z, Wang D, Wang D, Shu Y (2017). Simultaneous virus identification and characterization of severe unexplained pneumonia cases using a metagenomics sequencing technique. Science China. Life Sciences, 60(3): 279–286

RIGHTS & PERMISSIONS

Higher Education Press