Abstract
Salmonellosis is one of the most common causes of foodborne bacterial human disease worldwide, and the emergence of multidrug-resistant (MDR) strains of Salmonella enterica serovar Typhimurium (S. typhimurium) was associated to the incidence of invasive salmonellosis. The objective of the present work was to investigate the effects of the TiO2 photocatalysis process in terms of both bacteria inactivation and the emergence of mutants, on S. typhimurium TA102 water suspensions. The TiO2 photocatalysis was compared with a conventional disinfection process such as UV-C radiation. In spite of the faster bacterial inactivation obtained in UV-C disinfection experiments (45, 15, and 10 min for total inactivation for initial cell density 109, 108, and 107 CFU mL−1, respectively), photocatalytic disinfection (60, 30, and 15 min) was more energy efficient because of a lower energy requirement (2–20 mWs cm−2) compared to the UV-C disinfection process (5–30 mWs cm−2). During the photocatalytic experiments, the mutation frequency increased up to 1648-fold compared to background level for a 108 CFU mL−1 initial bacterial density, and mutants were inactivated after 1–10-min treatment, depending on initial bacterial cell density. In UV-C disinfection experiments, the mutation frequency increased up to 2181-fold for a 108 CFU mL−1 initial bacterial cell density, and UV-C doses in the range of 0.5–4.8 mWs cm−2 were necessary to decrease mutation frequency. In conclusion, both disinfection processes were effective in the inactivation of S. typhimurium cells, and mutants released into the environment can be avoided if cells are effectively inactivated.
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Berney HU, Weilenmann A, Simonetti T (2006) Efficacy of solar disinfection of Escherichia coli, Shigella flexneri, Salmonella typhimurium and Vibrio cholerae. J Appl Microbiol 101(4):828–836
Cho M, Chung H, Choi W, Yoon J (2004) Linear correlation between inactivation of E. coli and OH radical concentration in TiO2 photocatalytic disinfection. Water Res 38:1069–1077
Dalrymple OK, Stefanakos E, Trotz MA, Goswami DY (2010) A review of the mechanisms and modeling of photocatalytic disinfection. Appl Catalysis B: Environ 98:27–38
de Kok TM, van Maanen JM, Lankelma J, ten Hoor F, Kleinjans JC (1992) Electron spin resonance spectroscopy of oxygen radicals generated by synthetic fecapentaene-12 and reduction of fecapentaene mutagenicity to Salmonella typhimurium by hydroxyl radical scavenging. Carcinogenesis 13:1249–1255
Dunlop PSM, Ciavola M, Rizzo L, Byrne JA (2011) Inactivation and injury assessment of Escherichia coli during solar and photocatalytic disinfection in LDPE bags. Chemosphere 85:1160–1166
Fàbrega A, Vila J (2013) Salmonella enterica serovar typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 26(2):308–341
Foster HA, Ditta IB, Varghese S, Steele A (2011) Photocatalytic disinfection using titanium dioxide: spectrum and mechanism of antimicrobial activity. Appl Microbiol Biotechnol 90(6):1847–1868
Gordon MA, Graham SM, Walsh AL, Wilson LK, Phiri A, Molyneux EM et al (2008) Epidemics of invasive Salmonella enterica serovar enteritidis and Salmonella enterica serovar typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis 46:963–969
Grey CE, Adlercreutz P (2003) Ability of antioxidants to prevent oxidative mutations in Salmonella typhimurium TA102. Mutat Res 527:27–36
Grossweiner LI, Jones LR, Grossweiner JB, Rogers BHG (2005) Photochemical damage to biological systems. In The Science of Phototherapy: an Introduction (Ed Jones), Springer the Netherlands.
Haley BJ, Cole D (2009) Distribution, diversity, and seasonality of waterborne salmonellae in a rural watershed. Appl Environ Microb 75(5):1248–1255
Hignen WAM, Medema GJ (2006) Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Res 40(1):3–22
Kanno T, Nakamura K, Ikai H, Kikuchi K, Sasaki K, Niwano Y (2012) Literature review of the role of hydroxyl radicals in chemicallyinduced mutagenicity and carcinogenicity for the risk assessment of a disinfection system utilizing photolysis of hydrogen peroxide. J Clin Biochem Nutr 51:9–14
Koivunen J, Heinonen-Tanski H (2005) Inactivation of enteric microorganisms with chemical disinfectants, UV radiation and combined chemical/UV treatments. Water Res 39(8):1519–1526
Levantesi C, La Mantia R, Masciopinto C, Uta Böckelmann C et al (2010) Quantification of pathogenic microorganisms and microbial indicators in three wastewater reclamation and managed aquifer recharge facilities in Europe. Sci Total Environ 408(21):4923–4230
Levantesi C, Bonadonna L, Briancesco R, Grohmann E, Toze S, Tandoi V (2012) Salmonella in surface and drinking water: occurrence and water-mediated transmission. Food Res Int 45(2):587–602
Li H, Bhaskara A, Megalis C, Tortorello ML (2012) Transcriptomic analysis of Salmonella desiccation resistance. Foodborne Pathog Dis 9:1143–1151
Long M, Wang J, Zhuang H, Zhang Y, Wu H, Zhang J (2014) Performance and mechanism of standard nano-TiO2 (P-25) in photocatalytic disinfection of foodborne microorganisms—Salmonella typhimurium and Listeria monocytogenes. Food Control 39(1):68–74
Lu Z-X, Zhou L, Zhang Z-L, Shi W-L, Xie Z-X, Xie H-Y, Pang D-W, Shen P (2003) Cell damage induced by photocatalysis of TiO2 thin films. Langmuir 19:8765–8768
Magdeburg A, Stalter D, Schlsener M, Ternes T, Oehlmann J (2014) Evaluating the efficiency of advanced wastewater treatment: target analysis of organic contaminants and (geno-)toxicity assessment tell a different story. Water Res 50(0):35–47
Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, Jones TF, Fazil A, Hoekstra RM (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882–889
Maron DM, Ames BN (1983) Revised methods for Salmonella mutagenicity test. Mutat Res 101:173–215
Martinez-Urtaza J, Saco M, de Novoa J, Perez-Pineiro P, Peiteado J, Lozano-Leon A, Garcia-Martin O (2004) Influence of environmental factors and human activity on the presence of Salmonella serovars in a marine environment. Appl Environ Microbiol 70:2089–2097
Masarikova M, Manga I, Cizek A, Dolejska M, Oravcova V, Myskova P, Karpiskova R, Literak I (2016) Salmonella enterica resistant to antimicrobials in wastewater effluents and black-headed gulls in the Czech Republic, 2012. Sci Total Environ 542:102–107
McGuigan KG, Conroy RM, Mosler H-J, du Preez M, Ubomba-Jaswa E, Fernandez-Ibanez P (2012) Solar water disinfection (SODIS): a review from bench-top to roof-top. J Hazard Mater 235(236):29–46
Michael GB, Butaye P, Cloeckaert A, Schwarz S (2006) Genes and mutations conferring antimicrobial resistance in Salmonella: an update. Microbes Infect 8(7):1898–1914
Mišík M, Knasmueller S, Ferk F, Cichna-Markl M, Grummt T, Schaar H, Kreuzinger N (2011) Impact of ozonation on the genotoxic activity of tertiary treated municipalwastewatr. Water Res 45(12):3681–3691
Monarca S, Feretti D, Collivignarelli C, Guzzella G, Zerbini I, Bertanza G, Pedrazzani R (2000) The influence of different disinfectants on mutagenicity and toxicity of urban wastewater. Water Res 34(17):4261–4269
Nutt JD, Li X, Woodward CL, Zabala-Diaz IB, Ricke SC (2003) Growth kinetics response of a Salmonella typhimurium poultry marker strain to fresh produce extracts. Bioresource Technol 89:313–316
Oubrim N, Ennaji MM, Badri S, Cohen N (2012) Removal of antibiotic-resistant Salmonella in sewage water from wastewater treatment plants in Settat and Soualem, Morocco. Eur J Sci Res 68(4):565–573
Polo F, Figueras MJ, Inza I, Sala J, Fleisher JM, Guarro J (1999) Prevalence of Salmonella serotypes in environmental waters and their relationships with indicator organisms. A Van Leeuw 75:285–292
Polo-López MI, Castro-Alférez M, Oller I, Fernández-Ibáñez P (2014) Assessment of solar photo-Fenton, photocatalysis, and H2O2 for removal of phytopathogen fungi spores in synthetic and real effluents of urban wastewater. Chemi Eng J 257:122–130
Popoff MY (2001) Antigenic formulas of the salmonella serovars. In: WHO collaborating Center for Reference and Research on salmonella, 8th edn. Institut Pasteur Paris, France
Rahman BA, Wasfy MO, Maksoud MA, Hanna N, Dueger E, House B (2014) Multi-drug resistance and reduced susceptibility to ciprofloxacin among Salmonella enterica serovar typhi isolates from the Middle East and Central Asia. New Microbes and New Infect 2(4):88–92
Rahmani M, Peighambari SM, Svendsen CA, Cavaco LM, Agersø Y, Hendriksen RS (2013) Molecular clonality and antimicrobial resistance in Salmonella enterica serovars enteritidis and Infantis from broilers in three northern regions of Iran. BMC Vet Res 9:66
Rincon AG, Pulgarin C (2007) Fe3+ and TiO2 solar-light-assisted inactivation of E. coli at field scale—implications in solar disinfection at low temperature of large quantities of water. Catal Today 122:128–136
Rizzo L (2011) Bioassays as a tool for evaluating advanced oxidation processes in water and wastewater treatment. Water Res 45:4311–4330
Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360
Rizzo L, Ferro G, Manaia CM (2014a) Wastewater disinfection by solar heterogeneous photocatalysis: effect on tetracycline resistant/sensitive enterococcus strains. Global Nest J 16:455–462
Rizzo L, Della Sala A, Fiorentino A, Li Puma G (2014b) Disinfection of urban wastewater by solar driven and UV lamp-TiO2 photocatalysis: effect on a multi drug resistant Escherichia coli strain. Water Res 53:145–152
Robertson GP (2005) Functional and therapeutic significance of Akt deregulation in malignant melanoma. Cancer Metast Rev 24:273–285
Sciacca J, Rengifo-Herrera J, Wethe PC (2011) Solar disinfection of wild Salmonella sp. in natural water with a 18 L CPC photoreactor: detrimental effect of non-sterile storage of treated water. Sol Energy 85:1399–1408
Sharma VK, Johnson N, Cizmas L, McDonald TJ, Kim H (2016) A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere 150:702–714
Silva RC, Cardoso WM, Teixeira RSC, Albuquerque ÁH, Horn RV, Cavalcanti CM (2013) Salmonella Gallinarum virulence in experimentally infected Japanese quails (Coturnix japonica). Braz J of Poult Sci 15(1):39–45
Simonet J, Gantzer C (2006) Inactivation of poliovirus 1 and F-specific RNA phages and degradation of their genomes by UV irradiation at 254 nanometers. Appl Environ Microbiol 72(12):7671–7677
Sinha RP, Häder DP (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1(4):225–236
Tate P, Stannera A, Shieldsa K, Smithc S, Larcom L (2006) Blackberry extracts inhibit UV-induced mutagenesis in Salmonella typhimurium TA100. Nutr Res 26:100–104
Wang J, Zhuan H, Hinton A Jr, Bowker B, Zhang J (2014) Photocatalytic disinfection of spoilage bacteria Pseudomonas fluorescens and Macrococcus caseolyticus by nano-TiO2. LWT Food Sci Technol 59(2):1009–1017
Wéry N, Lhoutellier C, Ducray F, Delgenès JP, Godon JJ (2008) Behaviour of pathogenic and indicator bacteria during urban wastewater treatment and sludge composting, as revealed by quantitative PCR. Water Res 42:53–62
Acknowledgments
The support of University of Salerno through FARB2012 (Trattamento avanzato di acque reflue urbane mediante fotocatalisi: effetto sui batteri resistenti agli antibiotici) project funding is acknowledged. The authors would like also to acknowledge the financial support provided by COST-European Cooperation in Science and Technology, to the COST Action “TD0803: Detecting evolutionary hotspots of antibiotic resistances in Europe (DARE)” and COST Action “ES1403: New and emerging challenges and opportunities in wastewater reuse (NEREUS).” CM wishes to thank the “Zone Atelier Moselle” (ZAM) for supporting his research on treatment processes and their effects.
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Fiorentino, A., Rizzo, L., Guilloteau, H. et al. Comparing TiO2 photocatalysis and UV-C radiation for inactivation and mutant formation of Salmonella typhimurium TA102. Environ Sci Pollut Res 24, 1871–1879 (2017). https://doi.org/10.1007/s11356-016-7981-6
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DOI: https://doi.org/10.1007/s11356-016-7981-6