Legionella: Health Impacts, Exposure Evaluation, and Hazard Reduction

Djamel Ghernaout; Noureddine Elboughdiri; Ramzi Lajimi

doi:10.57056/ajet.v6i1.78

Authors

Djamel Ghernaout Chemical Engineering Department, College of Engineering, University of Ha’il, PO Box 2440, Ha’il 81441, Saudi Arabia, Chemical Engineering Department, Faculty of Engineering, University of Blida, PO Box 270, Blida 09000, Algeria
Noureddine Elboughdiri Chemical Engineering Department, College of Engineering, University of Ha’il, PO Box 2440, Ha’il 81441, Saudi Arabia, Chemical Engineering Process Department, National School of Engineers, Zrig Gabes 6029, University of Gabes, Gabes, Tunisia
Ramzi Lajimi Department of Chemistry, College of Science, University of Ha’il, P.O. Box 2440, Ha’il 81441, Saudi Arabia, Laboratory of Water, Membranes and Environmental Biotechnologies, Center of Researches and Water Technologies, PO Box 273, Soliman 8020, Tunisia

DOI:

https://doi.org/10.57056/ajet.v6i1.78

Keywords:

Legionella, Opportunistic pathogens, Pontiac fever, Legionnaires’ disease, Water treatment, Disinfection by-products

Abstract

Legionella pneumophila is an intracellular pathogen, omnipresent in the nature and seen as opportunistic. It is the main source of legionellosis that can take place in its nonpneumonic form (Pontiac fever) and acute pneumonic form (Legionnaires’ disease). In the aquatic systems, L. pneumophila can conquer and remain alive intracellularly in different protozoans. The faculty to multiply inside biofilms gives more safeguard from natural stresses like disinfection. Human contagion by L. pneumophila happens following the inhalation or aspiration of aerosols carrying the pathogen. This work defines microbiologically Legionella bacteria and presents a brief history relating to their first discovery and following contagions, a short description relating to their metabolism and physiology, a discussion of their clinical characteristics and their subsistence in the nature and growth in a biofilm, and a general examination of numerous technologies employed for their removal. The spread of opportunistic pathogens (OPs) remains the most significant feature of microbial potable water quality besides the generation of disinfection by-products (DBPs). The (re)growth of OPs and the production of DBPs in urban engineered water systems both closely correlate with the injections or concentrations of disinfectant residuals. Nonetheless, OPs and DBPs respond to disinfectant residuals frequently oppositely. An elevated residual concentration efficiently suppresses the (re)growth of OPs while intensifies the production of DBPs. Oppositely, a low or “detectable” disinfectant residual level decreases the generation of DBPs but could not stop OPs from thriving. To guarantee that the overall or combined health risks of OPs and DBPs are minimum, OP (re)growth and DBP generation must be deeply revised while selecting a practical disinfectant residual dosage or level.

References

Legionella (26/11/19). https://www.canada.ca/en/public-health/services/infectious-diseases/legionella.html (Accessed on 15/07/21).

Percival SL, Williams DW. Legionella. In Microbiology of waterborne diseases 2014 Jan 1 (pp. 155-175). Academic Press.

Gonçalves IG, Fernandes HS, Melo A, Sousa SF, Simões LC, Simões M. Legionella DB–A database on Legionella outbreaks. Trends in Microbiology. 2021;29(10):863-866.

Paranjape K, Bédard É, Whyte LG, Ronholm J, Prévost M, Faucher SP. Presence of Legionella spp. in cooling towers: the role of microbial diversity, Pseudomonas, and continuous chlorine application. Water Research. 2020;169:115252.

Napoli C, Iatta R, Fasano F, Marsico T, Montagna MT. Variable bacterial load of Legionella spp. in a hospital water system. Science of the total environment. 2009;408(2):242-244.

Costa J, da Costa MS, Veríssimo A. Colonization of a therapeutic spa with Legionella spp: a public health issue. Research in microbiology. 2010;161(1):18-25.

Liguori G, Di Onofrio V, Gallè F, Liguori R, Nastro RA, Guida M. Occurrence of Legionella spp. in thermal environments: Virulence factors and biofilm formation in isolates from a spa. Microchemical Journal. 2014;112:109-112.

Shaheen M, Scott C, Ashbolt NJ. Long-term persistence of infectious Legionella with free-living amoebae in drinking water biofilms. International Journal of Hygiene and Environmental Health. 2019;222(4):678-686.

Salinas MB, Fenoy S, Magnet A, Vaccaro L, Gomes TD, Angulo S, Hurtado C, Ollero D, Valdivieso E, del Águila C, Pozuelo MJ. Are pathogenic Legionella non-pneumophila a common bacteria in Water Distribution Networks?. Water Research. 2021;196:117013.

Schrammel B, Cervero-Aragó S, Dietersdorfer E, Walochnik J, Lück C, Sommer R, Kirschner A. Differential development of Legionella sub-populations during short-and long-term starvation. Water Research. 2018;141:417-427.

Cervero-Aragó S, Schrammel B, Dietersdorfer E, Sommer R, Lück C, Walochnik J, Kirschner A. Viability and infectivity of viable but nonculturable Legionella pneumophila strains induced at high temperatures. Water research. 2019;158:268-279.

Ditommaso S, Giacomuzzi M, Gentile M, Moiraghi AR, Zotti CM. Effective environmental sampling strategies for monitoring Legionella spp contamination in hot water systems. American journal of infection control. 2010;38(5):344-349.

Mansi A, Amori I, Marchesi I, Marcelloni AM, Proietto AR, Ferranti G, Magini V, Valeriani F, Borella P. Legionella spp. survival after different disinfection procedures: Comparison between conventional culture, qPCR and EMA–qPCR. Microchemical Journal. 2014;112:65-69.

Rodgers FG, Macrae AD, Lewis MJ. Electron microscopy of the organism of Legionnaires' disease. Nature. 1978;272(5656):825-256.

Wullings BA, Van Der Kooij D. Occurrence and genetic diversity of uncultured Legionella spp. in drinking water treated at temperatures below 15 C. Applied and Environmental Microbiology. 2006;72(1):157-166.

Pepper IL, Gerba CP. Risk of infection from Legionella associated with spray irrigation of reclaimed water. Water research. 2018;139:101-107.

Bollin GE, Plouffe JF, Para MF, Hackman B. Aerosols containing Legionella pneumophila generated by shower heads and hot-water faucets. Applied and environmental microbiology. 1985;50(5):1128-1131.

Chang CW, Chang WL, Chang ST. Influence of pH on bioactivity of cinnamon oil against Legionella pneumophila and its disinfection efficacy in hot springs. Water research. 2008;42(20):5022-5030.

Tatlock H. A rickettsia-like organism recovered from guinea pigs. Proceedings of the Society for Experimental Biology and Medicine. 1944;57(1):95-99.

Hookey JV, Saunders NA, Fry NK, Birtles RJ, Harrison TG. Phylogeny of Legionellaceae based on small-subunit ribosomal DNA sequences and proposal of Legionella lytica comb. nov. for Legionella-like amoebal pathogens. International Journal of Systematic and Evolutionary Microbiology. 1996;46(2):526-531.

Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, Sharrar RG, Harris J, Mallison GF, Martin SM, McDade JE, Shepard CC. Legionnaires' disease: description of an epidemic of pneumonia. New England Journal of Medicine. 1977;297(22):1189-1197.

Glick TH, Gregg MB, Berman B, Mallison G, RHODES JR WW, Kassanoff IR. Pontiac fever: an epidemic of unknown etiology in a health department: I. Clinical and epidemiologic aspects. American journal of epidemiology. 1978;107(2):149-160.

Steinert M, Ockert G, Lück C, Hacker J. Regrowth of Legionella pneumophila in a heat-disinfected plumbing system. Zentralblatt für Bakteriologie. 1998;288(3):331-342.

McDonough JA, Newton HJ, Roy CR. Coxiella burnetii secretion systems. Coxiella burnetii: Recent Advances and New Perspectives in Research of the Q Fever Bacterium. 2012:171-197.

Diederen BM. Legionella spp. and Legionnaires' disease. Journal of infection. 2008;56(1):1-2.

George JR, Pine L, Reeves MW, Harrell WK. Amino acid requirements of Legionella pneumophila. Journal of Clinical Microbiology. 1980;11(3):286-291.

Caterino U. Instability of gait as an extrapulmonary sequela in acute Legionella pneumonia: a case report. The Journal of Emergency Medicine. 2013;44(1):e13-15.

Yáñez MA, Carrasco-Serrano C, Barberá VM, Catalan V. Quantitative detection of Legionella pneumophila in water samples by immunomagnetic purification and real-time PCR amplification of the dotA gene. Applied and environmental microbiology. 2005;71(7):3433-3441.

Castilla J, Barricarte A, Aldaz J, Cenoz MG, Ferrer T, Pelaz C, Pineda S, Baladrón B, Martín I, Goñi B, Aratajo P. A large Legionnaires' disease outbreak in Pamplona, Spain: early detection, rapid control and no case fatality. Epidemiology & Infection. 2008;136(6):823-832.

Riffard S, Douglass S, Brooks T, Springthorpe S, Filion LG, Sattar SA. Occurrence of Legionella in groundwater: an ecological study. Water Science and Technology. 2001;43(12):99-102.

Devos L, Clymans K, Boon N, Verstraete W. Evaluation of nested PCR assays for the detection of Legionella pneumophila in a wide range of aquatic samples. Journal of Applied Microbiology. 2005;99(4):916-925.

Costa J, Tiago I, da Costa MS, Veríssimo A. Presence and persistence of Legionella spp. in groundwater. Applied and environmental microbiology. 2005;71(2):663-671.

Wang M, Ateia M, Awfa D, Yoshimura C. Regrowth of bacteria after light-based disinfection—What we know and where we go from here. Chemosphere. 2021;268:128850.

Oguma K, Katayama H, Ohgaki S. Photoreactivation of Legionella pneumophila after inactivation by low-or medium-pressure ultraviolet lamp. Water Research. 2004;38(11):2757-2763.

Zhang C, Lu J. Optimizing disinfectant residual dosage in engineered water systems to minimize the overall health risks of opportunistic pathogens and disinfection by-products. Science of The Total Environment. 2021;770:145356.

Mouchtouri V, Velonakis E, Hadjichristodoulou C. Thermal disinfection of hotels, hospitals, and athletic venues hot water distribution systems contaminated by Legionella species. American journal of infection control. 2007;35(9):623-627.

Marchesi I, Marchegiano P, Bargellini A, Cencetti S, Frezza G, Miselli M, Borella P. Effectiveness of different methods to control legionella in the water supply: ten-year experience in an Italian university hospital. Journal of Hospital Infection. 2011;77(1):47-51.

Yee RB, Wadowsky RM. Multiplication of Legionella pneumophila in unsterilized tap water. Applied and Environmental Microbiology. 1982;43(6):1330-1334.

Dennis PJ, Fitzgeorge RB, Taylor JA, Bartlett CL, Barrow GI. Legionella pneumophila in water plumbing systems. The Lancet. 1982;319(8278):949-51.

Barbaree JM, Fields BS, Feeley JC, Gorman GW, Martin WT. Isolation of protozoa from water associated with a legionellosis outbreak and demonstration of intracellular multiplication of Legionella pneumophila. Applied and Environmental Microbiology. 1986;51(2):422-424.

Breiman RF, Fields BS, Sanden GN, Volmer L, Meier A, Spika JS. Association of shower use with Legionnaires' disease: possible role of amoebae. Jama. 1990;263(21):2924-2926.

Cervero-Aragó S, Sommer R, Araujo RM. Effect of UV irradiation (253.7 nm) on free Legionella and Legionella associated with its amoebae hosts. Water research. 2014;67:299-309.

Chaúque BJ, Rott MB. Solar disinfection (SODIS) technologies as alternative for large-scale public drinking water supply: Advances and challenges. Chemosphere. 2021;281:130754.

Wadowsky RM, Butler LJ, Cook MK, Verma SM, Paul MA, Fields B, Keleti G, Sykora JL, Yee R. Growth-supporting activity for Legionella pneumophila in tap water cultures and implication of hartmannellid amoebae as growth factors. Applied and Environmental Microbiology. 1988;54(11):2677-2682.

Arslan-Aydoğdu EÖ, Kimiran A. An investigation of virulence factors of Legionella pneumophila environmental isolates. brazilian journal of microbiology. 2018;49:189-199.

Nakamura I, Amemura-Maekawa J, Kura F, Kobayashi T, Sato A, Watanabe H, Matsumoto T. Persistent Legionella contamination of water faucets in a tertiary hospital in Japan. International Journal of Infectious Diseases. 2020;93:300-304.

Alum A, Isaacs GZ. Aerobiology of the built environment: synergy between Legionella and fungi. American Journal of Infection Control. 2016;44(9):S138-S143.

Chen B, Han J, Dai H, Jia P. Biocide-tolerance and antibiotic-resistance in community environments and risk of direct transfers to humans: Unintended consequences of community-wide surface disinfecting during COVID-19?. Environmental Pollution. 2021;283:117074.

Rowbotham TJ. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. Journal of clinical pathology. 1980;33(12):1179-1183.

Gonçalves IG, Simões LC, Simões M. Legionella pneumophila. Trends Microbiol. 2021; 29:860–861

Macfarlane JT, Ward MJ, Finch RG, Macrae AD. HOSPITAL STUDY OF ADULT COMMUNITY-ACQUIRED PNEUMONIA. The Lancet. 1982;320(8292):255–258.

Kruse E-B, Wehner A, Wisplinghoff H. Prevalence and distribution of Legionella spp in potable water systems in Germany, risk factors associated with contamination, and effectiveness of thermal disinfection. American Journal of Infection Control. 2016;44(4):470–474

Altorkmany L, Kharseh M, Ljung A-L, Staffan Lundström T. Experimental and simulation validation of ABHE for disinfection of Legionella in hot water systems. Applied Thermal Engineering. 2017;116:253–265.

Arnow PM, Chou T, Weil D, Shapiro EN, Kretzschmar C. Nosocomial Legionnaires’ Disease Caused by Aerosolized Tap Water from Respiratory Devices. Journal of Infectious Diseases. 1982;146(4):460–467.

Mahoney FJ, Hoge CW, Farley TA, Barbaree JM, Breiman RF, Benson RF, et al. Communitywide outbreak of Legionnaires’ disease associated with a grocery store mist machine. The Journal of Infectious Diseases. 1992;165(4):736–739.

van der Lugt W, Euser SM, Bruin JP, den Boer JW, Yzerman EPF. Wide-scale study of 206 buildings in the Netherlands from 2011 to 2015 to determine the effect of drinking water management plans on the presence of Legionella spp. Water Research. 2019;161:581–589.

Polo-López MI, Castro-Alférez M, Nahim-Granados S, Malato S, Fernández-Ibáñez P. Legionella jordanis inactivation in water by solar driven processes: EMA-qPCR versus culture-based analyses for new mechanistic insights. Catalysis Today. 2017;287:15–21.

Lytle DA, Pfaller S, Muhlen C, Struewing I, Triantafyllidou S, White C, et al. A comprehensive evaluation of monochloramine disinfection on water quality, Legionella and other important microorganisms in a hospital. Water Research. 2021;189:116656.

Shen M, Zeng Z, Li L, Song B, Zhou C, Zeng G, et al. Microplastics act as an important protective umbrella for bacteria during water/wastewater disinfection. Journal of Cleaner Production. 2021;315:128188.

Declerck P, Behets J, van Hoef V, Ollevier F. Detection of Legionella spp. and some of their amoeba hosts in floating biofilms from anthropogenic and natural aquatic environments. Water Research. 2007;41(14):3159–3167.

Magnet A, Peralta RHS, Gomes TS, Izquierdo F, Fernandez-Vadillo C, Galvan AL, et al. Vectorial role of Acanthamoeba in Legionella propagation in water for human use. Science of The Total Environment. 2015;505:889–895.

Declerck P, Behets J, van Hoef V, Ollevier F. Replication of Legionella pneumophila in Floating Biofilms. Current Microbiology. 2007;55(5):435–40.

Kim BR, Anderson JE, Mueller SA, Gaines WA, Kendall AM. Literature review—efficacy of various disinfectants against Legionella in water systems. Water Research. 2002;36(18):4433–4444.

García MT, Jones S, Pelaz C, Millar RD, Abu Kwaik Y. Acanthamoeba polyphaga resuscitates viable non-culturable Legionella pneumophila after disinfection. Environmental Microbiology. 2007;9(5):1267–1277.

Fields BS, Benson RF, Besser RE. Legionella and Legionnaires’ Disease: 25 Years of Investigation. Clinical Microbiology Reviews. 2002;15(3):506–526..

Baron J, Harris J, Holinger E, Duda S, Stevens M, Robertson C et al. Effect of monochloramine treatment on the microbial ecology of Legionella and associated bacterial populations in a hospital hot water system. Systematic and Applied Microbiology. 2015;38(3):198-205.

Loret JF, Robert S, Thomas V, Lévi Y, Cooper AJ, McCoy WF. Comparison of disinfectants for biofilm, protozoa and Legionella control. Journal of Water and Health. 2005;3(4):423–433.

Vincenti S, de Waure C, Raponi M, Teleman A, Boninti F, Bruno S et al. Environmental surveillance of Legionella spp. colonization in the water system of a large academic hospital: Analysis of the four–year results on the effectiveness of the chlorine dioxide disinfection method. Science of The Total Environment. 2019;657:248-253.

Thomas V, Bouchez T, Nicolas V, Robert S, Loret JF, Levi Y. Amoebae in domestic water systems: resistance to disinfection treatments and implication in Legionella persistence. Journal of Applied Microbiology. 2004;97(5):950–963.

Donlan RM, Forster T, Murga R, Brown E, Lucas C, Carpenter J, et al. Legionella pneumophila associated with the protozoan Hartmannella vermiformisin a model multi-species biofilm has reduced susceptibility to disinfectants. Biofouling. 2005;21(1):1–7.

Casini B, Baggiani A, Totaro M, Mansi A, Costa AL, Aquino F, et al. Detection of viable but non-culturable legionella in hospital water network following monochloramine disinfection. Journal of Hospital Infection. 2018 ;98(1):46–52.

Triassi M, Popolo AD, D’Alcalà GR, Albanese Z, Cuccurullo S, Montegrosso S, et al. Clinical and environmental distribution of Legionella pneumophila in a university hospital in Italy: efficacy of ultraviolet disinfection. Journal of Hospital Infection .2006 ;62(4):494–501

Li N, Li X, Shi Z-Y, Fan X-Y, Zhou Z-W. Response of high-, mid- and low-abundant taxa and potential pathogens to eight disinfection methods and their interactions in domestic hot water system. Science of The Total Environment. 2020 ;749:141440.

Rattanakul S, Oguma K. Inactivation kinetics and efficiencies of UV-LEDs against Pseudomonas aeruginosa, Legionella pneumophila, and surrogate microorganisms. Water Research. 2018;130:31–37.

Declerck P, Vanysacker L, Hulsmans A, Lambert N, Liers S, Ollevier F. Evaluation of power ultrasound for disinfection of both Legionella pneumophila and its environmental host Acanthamoeba castellanii. Water Research. 2010;44(3):703–710.

Farshbaf Dadjour M, Ogino C, Matsumura S, Nakamura S, Shimizu N. Disinfection of Legionella pneumophila by ultrasonic treatment with TiO2. Water Research. 2006;40(6):1137–1142.

Cheng YW, Chan RCY, Wong PK. Disinfection of Legionella pneumophila by photocatalytic oxidation. Water Research. 2007 ;41(4):842–852.

hang C-W, Hwang Y-H, Cheng W-Y, Chang C-P. Effects of chlorination and heat disinfection on long-term starved Legionella pneumophila in warm water. Journal of Applied Microbiology. 2007;102(6):1636–1644.

Dobrowsky PH, Khan S, Khan W. Resistance of Legionella and Acanthamoeba mauritaniensis to heat treatment as determined by relative and quantitative polymerase chain reactions. Environmental Research. 2017;158:82–93.

Hsu SC, Martin R, Wentworth BB. Isolation of Legionella species from drinking water. Applied and Environmental Microbiology. 1984 ;48(4):830–832.

Steinert M, Emödy L, Amann R, Hacker J. Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Applied and environmental microbiology. 1997;63(5):2047–2053.

Ohno A, Kato N, Yamada K, Yamaguchi K. Factors Influencing Survival of Legionella pneumophila Serotype 1 in Hot Spring Water and Tap Water. Applied and Environmental Microbiology. 2003;69(5):2540–2547.

ooper IR, Hanlon GW. Resistance of Legionella pneumophila serotype 1 biofilms to chlorine-based disinfection. Journal of Hospital Infection. 2010;74(2):152–159.

He Z, Wang L, Ge Y, Zhang S, Tian Y, Yang X, et al. Both viable and inactivated amoeba spores protect their intracellular bacteria from drinking water disinfection. Journal of Hazardous Materials. 2021;417:126006.

Altorkmany L, Kharseh M, Ljung A, Staffan Lundström T. Effect of working parameters of the plate heat exchanger on the thermal performance of the anti-bact heat exchanger system to disinfect Legionella hot water systems. Applied Thermal Engineering. 2018;141:435-443.

Blanc D, Carrara P, Zanetti G, Francioli P. Water disinfection with ozone, copper and silver ions, and temperature increase to control Legionella: seven years of experience in a university teaching hospital. Journal of Hospital Infection. 2005;60(1):69-72.

Benakopoulos T, Tunzi M, Salenbien R, Vanhoudt D, Svendsen S. Low return temperature from domestic hot-water system based on instantaneous heat exchanger with chemical-based disinfection solution. Energy. 2021;215:119211.

Peiró Callizo E, Sierra J, Pombo J, Baquedano C, Huerta B. Evaluation of the effectiveness of the Pastormaster method for disinfection of legionella in a hospital water distribution system. Journal of Hospital Infection. 2005;60(2):150-158.

Papagianeli SD, Aspridou Z, Didos S, Chochlakis D, Psaroulaki A, Koutsoumanis K. Dynamic modelling of Legionella pneumophila thermal inactivation in water. Water Research. 2021;190:116743.

M.J. Lehtola, E. Torvinen, J. Kusnetsov, T. Pitkänen, L. Maunula, C.H. von Bonsdorff, P.J. Martikainen, S.A. Wilks, C.W. Keevil, I.T. Miettinen, Survival of Mycobacterium avium, Legionella pneumophila, Escherichia coli, and caliciviruses in drinking water-associated biofilms grown under high-shear turbulent flow. Applied and Environmental Microbiology. 2007;73(9): 2854-2859.

caturro M, Dell’Eva I, Helfer F, Ricci ML. Persistence of the Same Strain of Legionella pneumophila in the Water System of an Italian Hospital for 15 Years. Infection Control & Hospital Epidemiology. 2007;28(9):1089–1092.

Rasheduzzaman M, Singh R, Haas C, Gurian P. Required water temperature in hotel plumbing to control Legionella growth. Water Research. 2020;182:115943.

Cachafeiro S, Naveira I, García I. Is copper–silver ionisation safe and effective in controlling legionella?. Journal of Hospital Infection. 2007;67(3):209-216.

Kessler M, Osman F, Marx J, Pop-Vicas A, Safdar N. Hospital-acquired Legionella pneumonia outbreak at an academic medical center: Lessons learned. American Journal of Infection Control. 2021;49(8):1014-1020.

Goetz A, Yu V. Copper-silver ionization: Cautious optimism for Legionella disinfection and implications for environmental culturing. American Journal of Infection Control. 1997;25(6):449-451.

Amara S, Baghdadli T, Knapp S, Nordell B. Legionella disinfection by solar concentrator system. Renewable and Sustainable Energy Reviews. 2017;70:786–792.

Cao K, Chen Z, Shi Q, Wu Y, Lu Y, Mao Y et al. An insight to sequential ozone chlorine process for synergistic disinfection on reclaimed water: Experimental and modelling studies. Science of The Total Environment. 2021;793:148563.

Li J, Li K, Zhou Y, Li X, Tao T. Kinetic analysis of Legionella inactivation using ozone in wastewater. Chemosphere. 2017;168:630-637.

Pinel I, Hankinson P, Moed D, Wyseure L, Vrouwenvelder J, van Loosdrecht M. Efficient cooling tower operation at alkaline pH for the control of Legionella pneumophila and other pathogenic genera. Water Research. 2021;197:117047.

Delaedt Y, Daneels A, Declerck P, Behets J, Ryckeboer J, Peters E et al. The impact of electrochemical disinfection on Escherichia coli and Legionella pneumophila in tap water. Microbiological Research. 2008;163(2):192-199.

Furuta T, Tanaka H, Nishiki Y, Pupunat L, Haenni W, Rychen P. Legionella inactivation with diamond electrodes. Diamond and Related Materials. 2004;13(11-12):2016-2019.

Martínez-Huitle CA, Brillas E. A critical review over the electrochemical disinfection of bacteria in synthetic and real wastewaters using a boron-doped diamond anode. Current Opinion in Solid State and Materials Science. 2021;25(4):100926.

Feng C, Suzuki K, Zhao S, Sugiura N, Shimada S, Maekawa T. Water disinfection by electrochemical treatment. Bioresource technology. 2004;94(1):21-25.

Bonetta S, Pignata C, Bonetta S, Meucci L, Giacosa D, Marino E, Gorrasi I, Gilli G, Carraro E. Effectiveness of a neutral electrolysed oxidising water (NEOW) device in reducing Legionella pneumophila in a water distribution system: A comparison between culture, qPCR and PMA-qPCR detection methods. Chemosphere. 2018;210:550-556.

Montenegro-Ayo R, Barrios AC, Mondal I, Bhagat K, Morales-Gomero JC, Abbaszadegan M, Westerhoff P, Perreault F, Garcia-Segura S. Portable point-of-use photoelectrocatalytic device provides rapid water disinfection. Science of the Total Environment. 2020;737:140044.

Jeong E, Park HY, Lee J, Kim HE, Lee C, Kim EJ, Hong SW. Long-term and stable antimicrobial properties of immobilized Ni/TiO2 nanocomposites against Escherichia coli, Legionella thermalis, and MS2 bacteriophage. Environmental Research. 2021;194:110657.

De Battisti A, Formaglio P, Ferro S, Al Aukidy M, Verlicchi P. Electrochemical disinfection of groundwater for civil use–An example of an effective endogenous advanced oxidation process. Chemosphere. 2018;207:101-109.

Muzzi A, Cutti S, Bonadeo E, Lodola L, Monzillo V, Corbella M, Scudeller L, Novelli V, Marena C. Prevention of nosocomial legionellosis by best water management: Comparison of three decontamination methods. Journal of Hospital Infection. 2020;105(4):766-772.

Sun X, Liu J, Ji L, Wang G, Zhao S, Yoon JY, Chen S. A review on hydrodynamic cavitation disinfection: The current state of knowledge. Science of the Total Environment. 2020;737:139606.

Šarc A, Oder M, Dular M. Can rapid pressure decrease induced by supercavitation efficiently eradicate Legionella pneumophila bacteria?. Desalination and Water Treatment. 2016;57(5):2184-2194.

Caicedo C, Rosenwinkel KH, Exner M, Verstraete W, Suchenwirth R, Hartemann P, Nogueira R. Legionella occurrence in municipal and industrial wastewater treatment plants and risks of reclaimed wastewater reuse. Water research. 2019;149:21-34.

Dong S, Li J, Kim MH, Cho J, Park SJ, Nguyen TH, Eden JG. Deactivation of Legionella Pneumophila in municipal wastewater by ozone generated in arrays of microchannel plasmas. Journal of Physics D: Applied Physics. 2018;51(25):255501..

Hu D, Hong H, Rong B, Wei Y, Zeng J, Zhu J, Bai L, Guo F, Yu X. A comprehensive investigation of the microbial risk of secondary water supply systems in residential neighborhoods in a large city. Water Research. 2021;205:117690.

Chen GQ, Wu YH, Wang YH, Chen Z, Tong X, Bai Y, Luo LW, Xu C, Hu HY. Effects of microbial inactivation approaches on quantity and properties of extracellular polymeric substances in the process of wastewater treatment and reclamation: A review. Journal of Hazardous Materials. 2021;413:125283.