Effect of Ozone Micronano Bubbles on the Removal of Infectious Pathogens in Contaminated Water: Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, and Enterococcus faecalis
Publication: Journal of Environmental Engineering
Volume 150, Issue 3
Abstract
The present study was performed to explore the bactericidal effect of ozone micronano bubbles (OMNBs) against Pseudomonas aeruginosa, Escherichia coli (as gram-negative bacteria), Enterococcus faecalis, and Staphylococcus aureus (gram-positive bacteria). The effects of conventional ozonation (CO) or macrobubbles were also investigated for comparison. Three rates of ozone (10, 5, and ) in both forms (OMNB and CO) were employed in different time contacts. Samples were collected at different contact times. The most significant bactericidal effect of OMNB was observed in P. aeruginosa and S. aureus at ozone, which killed 100% of these bacteria after 8 and 5 min, respectively, whereas the kill times by CO at the same rates were 120 min for P. aeruginosa and 90 min for S. aureus, E. coli, and E. faecalis showed the same pattern of kill time, 60 and 60 min by CO and 3 and 2 min by OMNB, respectively. Results showed that the removal efficiency was significantly increased compared to the ordinary ozonation at the same ozone rates. According to the results of this study, disinfection of water contaminated with these bacteria can be effectively performed using OMNBs to accelerate and increase the efficiency of the disinfection process. The results may open a new horizon to disinfect medical and food processing instruments and surfaces more effectively without remaining residuals and harm to the environment.
Get full access to this article
View all available purchase options and get full access to this article.
Data Availability Statement
The authors declare that the data supporting the findings of this study are available within the paper and its supplementary information file. If any raw data files are needed in another format, they are available from the corresponding author upon reasonable request.
Acknowledgments
This article was extracted from an MSc thesis by Niloofar Gohari and was supported by the funding from Shahroud University of Technology, Iran.
References
Alwi, N., and A. Ali. 2014. “Reduction of Escherichia coli O157, Listeria monocytogenes and Salmonella enterica sv. Typhimurium populations on fresh-cut bell pepper using gaseous ozone.” Food Control 46 (Dec): 304–311. https://doi.org/10.1016/j.foodcont.2014.05.037.
Ananthanarayan, R., and C. K. J. Paniker. 2005. Textbook of microbiology. 7th ed. Hyderabad, India: Orient Longman Private.
Asadollahfardi, G., P. MohsenZadeh, S. F. Saghravani, and N. Mohamadzadeh. 2019. “The effects of using metakaolin and micro-nanobubble water on concrete properties.” J. Build. Eng. 25 (Sep): 1–35. https://doi.org/10.1016/j.jobe.2019.100781.
Brooks, G., K. Carroll, J. Butel, S. Mores, and T. Mietzner. 2013. Jawetz, Melnick and Adelberg, medical microbiology. 26th ed. New York: McGraw Hill.
Dahrazma, B., A. Naghedinia, H. Ghasemian Gorgi, and S. F. Saghravani. 2019. “Morphological and physiological responses of Cucumis sativus L. to water with micro-nanobubbles.” J. Agric. Sci. Technol. 21 (1): 181–192.
Dancer, S. 2014. “Controlling hospital-acquired infection: Focus on the role of the environment and new technologies for decontamination.” Clin. Microbiol. Rev. 27 (4): 665–690. https://doi.org/10.1128/CMR.00020-14.
Ebina, K., K. Shi, M. Hirao, J. Hashimoto, Y. Kawato, S. Kaneshiro, T. Morimoto, K. Koizumi, and H. Yoshikawa. 2013. “Oxygen and air nanobubble water solution promote the growth of plants, fishes, and mice.” Public Lib. Sci. 8 (6): 1–7. https://doi.org/10.1371/journal.pone.0065339.
Ebrahimi, H., M. Karamoozian, and S. F. Saghravani. 2020. “Interaction of applying stable micro-nano bubbles and ultrasonic irradiation in coal flotation.” Int. J. Coal Prep. Util. 42 (5): 1548–1562. https://doi.org/10.1080/19392699.2020.1732947.
Ersoy, Z. G., S. Barisci, and O. Dinc. 2019. “Mechanisms of the Escherichia coli and Enterococcus faecalis inactivation by ozone.” LWT 100 (Feb): 306–313. https://doi.org/10.1016/j.lwt.2018.10.095.
Farajzadehha, S., J. Shayegan, and F. Saghravani. 2022. “Pilot-scale study of hydraulic retention time and energy consumption in biological treatment of raw municipal wastewater by air micro-nanobubble aeration in different seasons.” Desalin. Water Treat. 280 (Dec): 9–18. https://doi.org/10.5004/dwt.2022.29032.
Ghadimkhani, A., T. Marhaba, and W. Zhang. 2016. “Ceramic membrane defouling (cleaning) by air nano bubbles.” Chemosphere 146 (Mar): 379–384. https://doi.org/10.1016/j.chemosphere.2015.12.023.
Giménez, B., N. Graiver, L. Giannuzzi, and N. Zaritzky. 2021. “Treatment of beef with gaseous ozone: Physicochemical aspects and antimicrobial effects on heterotrophic microflora and listeria monocytogenes.” Food Control 121 (Mar): 107602. https://doi.org/10.1016/j.foodcont.2020.107602.
Hu, L., and Z. Xia. 2018. “Application of ozone micro-nano-bubbles to groundwater Remediation.” J. Hazard. 342 (Jan): 446–453. https://doi.org/10.1016/j.jhazmat.2017.08.030.
ICMSF (International Commission on Microbiological Specifications for Foods). 1996. Microorganisms in food 5, characteristics of microbial pathogens. London: Blackie Academic & Professional.
Inatsu, Y., T. Kitagawa, N. Nakamura, S. Kawasaki, D. Nei, L. Bari, and S. Kawamoto. 2011. “Effectiveness of stable ozone micro bubble water on reducing bacteria on the surface of selected leafy vegetables.” Food Sci. Technol. Res. 17 (6): 479–485. https://doi.org/10.3136/fstr.17.479.
Jiang, C., S. Zhao, W. Song, T. Yamaguchi, and G. Riskowski. 2016. “Effect of micro-nano bubble water on growth, yield and quality of lettuce under substrate cultivation.” Int. Agric. Eng. J. 25 (3): 1–8.
Karaca, H., and Y. Velioglu. 2020. “Effects of ozone and chlorine washes and subsequent cold storage on microbiological quality and shelf life of fresh parsley leaves.” LWT 127 (Jun): 109421. https://doi.org/10.1016/j.lwt.2020.109421.
Kumar, M. 2016. “Ozone nano bubble water: A magic wand for the treatment of periodontal disease.” ARC J. Dental Sci. 1 (3): 1–2.
Li, Y., Y. Liu, Y. Zhou, T. Wang, J. Pan, B. Zhou, T. Muhammad, and C. Zhou. 2019. “Micro-nano bubble water oxygation: Synergistically improving irrigation water use efficiency, crop yield and quality.” J. Cleaner Prod. 222 (Jun): 835–843. https://doi.org/10.1016/j.jclepro.2019.02.208.
Malkutian, M., R. Dehghanzadeh Rihani, S. Satarvand, and M. Luluui. 2014. “Efficiency of ozonation and advanced oxidation in removing coliform bacteria from raw hospital wastewater.” [In Persian.] J. Rafsanjan Univ. Med. Sci. 14 (8): 679–690.
Matsuki, N., T. Ishikawa, S. Ichiba, N. Shiba, Y. Ujike, and T. Yamaguchi. 2014. “Oxygen supersaturated fluid using fine micro-nano bubbles.” Int. J. Nanomed. 20: 4495–4505. https://doi.org/10.2147/IJN.S68840.
McFarland, J. 1907. “Nephelometer; an instrument for estimating the number of bacteria in suspension used for calculating the opsonic index and for vaccines.” J. Am. Med. Assoc. XLIX (14): 1176–1178. https://doi.org/10.1001/jama.1907.25320140022001f.
Metcalf, L., H. Eddy, G. Tchobanoglous, F. Burton, and H. D. Stense. 2004. Wastewater engineering treatment, disposal and reuse. 4th ed. New York: McGraw Hill Higher Education.
Mohsenzadeh, P., S. F. Saghravani, and G. Asadollahfardi. 2018. “Mechanical and durability properties of concrete containing zeolite mixed with meta-kaolin and micro-nano bubbles of water.” Struct. Concr. 20 (2): 786–797. https://doi.org/10.1002/suco.201800030.
Morimoto, Y., A. Yoshida, S. Murakami, H. Tsuji, T. Yoshitaka, and T. Ozaki. 2010. “Micronano bubble containing ozone is efficient for bacterial biofilms on orthopaedic material.” In Proc., 56th Annual Meeting of the Orthopaedic Research Society, Poster No.2147. Tokyo, Japan: National Research Institute for Child Health and Development.
Nakatake, Y., S. Kisu, K. Shigyo, T. Eguchi, and T. Watanabe. 2013. “Effect of nano air-bubbles mixed into gas oil on common-raildiesel engine.” Energy 59 (Sep): 233–239. https://doi.org/10.1016/j.energy.2013.06.065.
Oh, J., D. E. Salcedo, C. A. Medriano, and S. Kim. 2014. “Comparison of different disinfection processes in the effective removal of antibiotic-resistant bacteria and genes.” J. Environ. Sci. 26 (6): 1238–1242. https://doi.org/10.1016/S1001-0742(13)60594-X.
Oh, K. S., P. E. Poh, M. N. Chong, D. Gouwanda, W. H. Lam, and C. Y. Chee. 2015. “Optimizing the in-line ozone injection and delivery strategy in a multistage pilot-scale greywater treatment system: System validation and cost-benefit analysis.” J. Environ. Chem. Eng. 3 (2): 1146–1151. https://doi.org/10.1016/j.jece.2015.04.022.
Price, R., and D. Wildeboer. 2017. “E. coli as an indicator of contamination and health risk in environmental waters.” In Escherichia coli, edited by A. Samie. London: IntechOpen.
Rajam, R., R. Harish, S. Guru Prasad, and S. Ramanathan. 2016. “Nano bubbles.” Br. J. Pharm. Med. Res. 1 (2): 72–79.
Ramsey, M., A. Hartke, and M. Huycke. 2014. Enterococci, from commensals to leading causes of drug resistant infection. Boston: Massachusetts Eye and Ear Infirmary.
Rojas-Valencia, M. N. 2011. “Research on ozone application as disinfectant and action mechanisms on wastewater microorganisms.” In Science against microbial pathogens: Communicating current research and technological advances, edited by A. Méndez-Vilas, 263–271. Extremadura, Spain: Formatex Research Center.
Rostami, H., H. Tawakli, R. Ranjbar, M. Delkhosh, M. Noorabadi, F. Rostami, and J. Yazdani. 2009. “Investigating the effect of ozone gas in reducing the overall bacterial consumption of chicken carcasses grown in one of the industrial slaughterhouses in Tehran.” [In Persian.] Iranian J. Med. Microbiol. 4 (4): 66–74.
Sakr, M., M. Mohamed, M. Maraqa, M. Hamouda, A. Aly Hassan, J. Ali, and J. Jung. 2022. “A critical review of the recent developments in micro–nano bubbles applications for domestic and industrial wastewater treatment Marwa.” Alexandria Eng. J. 61 (8): 6591–6612. https://doi.org/10.1016/j.aej.2021.11.041.
Seki, M., T. Ishikawa, H. Terada, and M. Nashimoto. 2017. “Microbicidal effects of stored aqueous ozone solution generated by nano-bubble technology.” Res. Inst. Healthy Living 31 (4): 570–583.
Serizawa, A. 2017. “Fundamentals and applications of micro/nano bubbles.” In Proc., 1st International Symposium on Application of High voltage, Plasmas & Micro/Nano Bubbles to Agriculture and Aquaculture. Chiang Mai, Thailand: Rajamangala Univ. of Technology.
Stange, C., J. P. S. Sidhu, S. Toze, and A. Tiehm. 2019. “Comparative removal of antibiotic resistance genes during chlorination, ozonation, and UV treatment.” Int. J. Hyg. Environ. Health 222 (3): 541–548. https://doi.org/10.1016/j.ijheh.2019.02.002.
Stewart, C. M. 2003. “Staphylococcus aureus and staphylococcal enterotoxins.” In Foodborne microorganisms of public health significance, 359–376. Waterloo, Canada: Australian Institute of Food Science and Technology.
Sumikura, M., M. Hidaka, H. Murakami, Y. Nobutomo, and T. Murakami. 2007. “Ozone micro-nano bubble disinfection method for wastewater reuse system.” Water Sci. Technol. 56 (5): 53–61. https://doi.org/10.2166/wst.2007.556.
Taherpour Komishani, F., S. F. Saghravani, and M. Jalali. 2020. “Effect of seawater on micro-nano air bubbles concrete for repair of coastal structures.” J. Rehabil. Civ. Eng. 8 (3): 34–42. https://doi.org/10.22075/JRCE.2020.18723.1354.
Torlak, E., D. Sert, and P. Ulca. 2013. “Efficacy of gaseous ozone against Salmonella and microbial population on dried oregano.” Int. J. Food Microbiol. 165 (3): 276–280. https://doi.org/10.1016/j.ijfoodmicro.2013.05.030.
Tsuge, H. 2014. Micro and nano bubbles fundamentals and applications. London: CRC Press.
Ushida, A., T. Koyama, Y. Nakamoto, T. Narumi, T. Sato, and T. Hasegawa. 2017. “Antimicrobial effectiveness of ultra-fine ozone-rich bubble mixtures for fresh vegetables using an alternating flow.” J. Food Eng. 206 (Aug): 48–56. https://doi.org/10.1016/j.jfoodeng.2017.03.003.
Xiao, H., T. Aftab, and D. Li. 2019. “Applications of micro-nano bubble technology in environmental pollution control.” Micro Nano Lett. 14 (7): 782–787. https://doi.org/10.1049/mnl.2018.5710.
Information & Authors
Information
Published In
Journal of Environmental Engineering
Volume 150 • Issue 3 • March 2024
Copyright
© 2024 American Society of Civil Engineers.
History
Received: Jun 23, 2023
Accepted: Nov 2, 2023
Published online: Jan 9, 2024
Published in print: Mar 1, 2024
Discussion open until: Jun 9, 2024
ASCE Technical Topics:
Authors
Metrics & Citations
Metrics
Citations
Download citation
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.