Abstract
Bioaerosol emission from aeration ponds of wastewater treatment plants can cause serious health effects on staff and associated personnel. Therefore, this research focused on estimating the acceptable level of exposure to two bioindicators, mainly Staphylococcus aureus and Gram-negative bacteria bioaerosols for staff and associated personnel researchers. To do so, a reverse quantitative microbial risk assessment approach was used based on an annual infection risk benchmark. The results showed that the estimations of the acceptable exposure time for aerosolized Gram-negative bacteria and Staphylococcus aureus were similar. For each specific exposure scenario, the acceptable exposure time for males was always shorter than that for females. To satisfy the official recommended on-site working time, wearing N-95 masks should be mandatory for staff and researchers under the inverted umbrella aeration mode in the H wastewater treatment plant and the fine-pore aeration mode in the T wastewater treatment plant. Nevertheless, under the fine-pore aeration mode in the H wastewater treatment plant, the recommended working time was satisfied even for the worst estimate. In addition, the acceptable exposure time of the beta-Poisson dose–response model showed an order of magnitude shorter than that of the exponential dose–response model. In general, these reverse quantitative microbial risk assessment results could deliver a feasible guideline for directly helping the exposure population to control their exposure time and manage their health risks in wastewater treatment plants, as well as help decision-makers to regulate the recommended working time.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amoueyan E, Ahmad S, Eisenberg JNS, Gerrity D (2019) Equivalency of indirect and direct potable reuse paradigms based on a quantitative microbial risk assessment framework. Microb Risk Anal 12:60–75. https://doi.org/10.1016/j.mran.2019.06.003
Armitage P, Spicer CC (1956) The detection of variation in host susceptibility in dilution counting experiments. J Hyg (lond) 54:401–414. https://doi.org/10.1017/S0022172400044661
Armstrong TW, Haas CN (2007) A quantitative microbial risk assessment model for Legionnaires’ disease: animal model selection and dose-response modeling. Risk Anal 27:1581–1596. https://doi.org/10.1111/j.1539-6924.2007.00990.x
Bauer H, Fuerhacker M, Zibuschka F et al (2002) Bacteria and fungi in aerosols generated by two different types of wastewater treatment plants. Water Res 36:3965–3970. https://doi.org/10.1016/S0043-1354(02)00121-5
Blanky M, Sharaby Y, Rodríguez-Martínez S et al (2017) Greywater reuse assessment of the health risk induced by Legionella pneumophila. Water Res 125:410–417. https://doi.org/10.1016/j.watres.2017.08.068
Bragoszewska E, Biedroń I (2018) Indoor air quality and potential health risk impacts of exposure to antibiotic resistant bacteria in an office rooms in southern poland. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph15112604
Brandi G, Sisti M, Amagliani G (2000) Evaluation of the environmental impact of microbial aerosols generated by wastewater treatment plants utilizing different aeration systems. J Appl Microbiol 88:845–852. https://doi.org/10.1046/j.1365-2672.2000.01024.x
Buonanno G, Morawska L, Stabile L (2020) Quantitative assessment of the risk of airborne transmission of SARS-CoV-2 infection: Prospective and retrospective applications. Environ Int 145:106112
Burdsall AC, Xing Y, Cooper CW, Harper WF (2021) Bioaerosol emissions from activated sludge basins: characterization, release, and attenuation. Sci Total Environ 753:141852. https://doi.org/10.1016/j.scitotenv.2020.141852
Busgang A, Friedler E, Gilboa Y, Gross A (2018) Quantitative microbial risk analysis for various bacterial exposure scenarios involving greywater reuse for irrigation. Water (switzerland) 10:1–15. https://doi.org/10.3390/w10040413
Carducci A, Donzelli G, Cioni L, Verani M (2016) Quantitative microbial risk assessment in occupational settings applied to the airborne human adenovirus infection. Int J Environ Res Public Health 13:733. https://doi.org/10.3390/ijerph13070733
Carducci A, Donzelli G, Cioni L et al (2018) Quantitative microbial risk assessment for workers exposed to bioaerosol in wastewater treatment plants aimed at the choice and setup of safety measures. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph15071490
Chappell WR (1992) Scaling toxicity data across species. Environ Geochem Health 14:71–80. https://doi.org/10.1007/BF01784017
Dean K, Mitchell J (2020) Reverse QMRA for Pseudomonas aeruginosa in premise plumbing to inform risk management. J Environ Eng 146:04019120. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001641
Douwes J, Thorne P, Pearce N, Heederik D (2003) Bioaerosol health effects and exposure assessment: progress and prospects. Ann Occup Hyg 47:187–200. https://doi.org/10.1093/annhyg/meg032
Dungan RS (2014) Estimation of infectious risks in residential populations exposed to airborne pathogens during center pivot irrigation of dairy wastewaters. Environ Sci Technol 48:5033–5042. https://doi.org/10.1021/es405693v
Esfahanian E, Adhikari U, Dolan K, Mitchell J (2019) Construction of a new dose- response model for Staphylococcus aureus considering growth and decay kinetics on skin. Pathogens. https://doi.org/10.3390/pathogens8040253
Fathi S, Hajizadeh Y, Nikaeen M, Gorbani M (2017) Assessment of microbial aerosol emissions in an urban wastewater treatment plant operated with activated sludge process. Aerobiol (bol) 33:507–515. https://doi.org/10.1007/s10453-017-9486-2
Ferguson R, Charlotte EEN, Zaheer AN et al (2020) Size fractionation of bioaerosol emissions from green-waste composting. Environ Int. https://doi.org/10.1016/j.envint.2020.106327
Fernando NL, Fedorak PM (2005) Changes at an activated sludge sewage treatment plant alter the numbers of airborne aerobic microorganisms. Water Res 39:4597–4608. https://doi.org/10.1016/j.watres.2005.08.010
Fracchia L, Pietronave S, Rinaldi M, Giovanna Martinotti M (2006) Site-related airborne biological hazard and seasonal variations in two wastewater treatment plants. Water Res 40:1985–1994. https://doi.org/10.1016/j.watres.2006.03.016
Fry FA, Black A (1973) Regional deposition and clearance of particles in the human nose. J Aerosol Sci. https://doi.org/10.1016/0021-8502(73)90063-3
Grzyb J, Lenart-Boroń A (2019) Bacterial bioaerosol concentration and size distribution in the selected animal premises in a zoological garden. Aerobiol (bol) 35:253–268. https://doi.org/10.1007/s10453-018-09557-9
Guo X, Wu P, Ding W et al (2014) Reduction and characterization of bioaerosols in a wastewater treatment station via ventilation. J Environ Sci (china) 26:1575–1583. https://doi.org/10.1016/j.jes.2014.06.001
Haas CN (2015) Microbial dose response modeling: past, present, and future. Environ Sci Technol 49:1245–1259. https://doi.org/10.1021/es504422q
Haas C, Rycroft T, Bibby K, Casson L (2017) Risks from ebolavirus discharge from hospitals to sewer workers. Water Environ Res 89:357–368. https://doi.org/10.2175/106143017x14839994523181
Hamilton AJ, Stagnitti F, Premier R et al (2006) Quantitative microbial risk assessment models for consumption of raw vegetables irrigated with reclaimed water. Appl Environ Microbiol 72:3284–3290. https://doi.org/10.1128/AEM.72.5.3284-3290.2006
Hamilton MA, Hong T, Casman E, Gurian PL (2015) Risk-based decision making for reoccupation of contaminated areas following a wide-area anthrax release. Risk Anal 35:1348–1363. https://doi.org/10.1111/risa.12383
Hamilton KA, Hamilton MT, Johnson W et al (2019) Risk-based critical concentrations of Legionella pneumophila for indoor residential water uses. Environ Sci Technol 53:4528–4541. https://doi.org/10.1021/acs.est.8b03000
Han Y, Li L, Liu J (2013) Characterization of the airborne bacteria community at different distances from the rotating brushes in a wastewater treatment plant by 16S rRNA gene clone libraries. J Environ Sci (china) 25:5–15. https://doi.org/10.1016/S1001-0742(12)60018-7
Han Y, Yang K, Yang T et al (2019) Bioaerosols emission and exposure risk of a wastewater treatment plant with A2O treatment process. Ecotoxicol Environ Saf 169:161–168. https://doi.org/10.1016/j.ecoenv.2018.11.018
Howard G, Pedley S, Tibatemwa S (2006) Quantitative microbial risk assessment to estimate health risks attributable to water supply: can the technique be applied in developing countries with limited data? J Water Health 4:49–65. https://doi.org/10.2166/wh.2006.0004
Hung HF, Kuo YM, Chien CC, Chen CC (2010) Use of floating balls for reducing bacterial aerosol emissions from aeration in wastewater treatment processes. J Hazard Mater 175:866–871. https://doi.org/10.1016/j.jhazmat.2009.10.090
Jahne MA, Rogers SW, Holsen TM, Grimberg SJ (2015) Quantitative microbial risk assessment of bioaerosols from a manure application site. Aerobiol (bol) 31:73–87. https://doi.org/10.1007/s10453-014-9348-0
Jahne MA, Rogers SW, Holsen TM et al (2016) Bioaerosol deposition to food crops near manure application: quantitative microbial risk assessment. J Environ Qual 45:666–674. https://doi.org/10.2134/jeq2015.04.0187
Korzeniewska E (2011) Emission of bacteria and fungi in the air from wastewater treatment plants: a review. Front Biosci S3:393–407
Kowalski M, Wolany J, Pastuszka JS et al (2017) Characteristics of airborne bacteria and fungi in some polish wastewater treatment plants. Int J Environ Sci Technol 14:2181–2192. https://doi.org/10.1007/s13762-017-1314-2
Kummer V, Thiel WR (2008) Bioaerosols-sources and control measures. Int J Hyg Environ Health 211:299–307. https://doi.org/10.1016/j.ijheh.2007.06.006
Lee H, Kim K, Choi KH, Yoon Y (2015) Quantitative microbial risk assessment for Staphylococcus aureus in natural and processed cheese in Korea. J Dairy Sci 98:5931–5945. https://doi.org/10.3168/jds.2015-9611
Li L, Han Y, Liu J (2013) Assessing genetic structure, diversity of bacterial aerosol from aeration system in an oxidation ditch wastewater treatment plant by culture methods and bio-molecular tools. Environ Monit Assess 185:603–613. https://doi.org/10.1007/s10661-012-2578-0
Lim KY, Hamilton AJ, Jiang SC (2015) Assessment of public health risk associated with viral contamination in harvested urban stormwater for domestic applications. Sci Total Environ 523:95–108. https://doi.org/10.1016/j.scitotenv.2015.03.077
Macler BA, Regli S (1993) Use of microbial risk assessment in setting US drinking water standards. Int J Food Microbiol 18:245–256. https://doi.org/10.1016/0168-1605(93)90148-A
Malakootian M, Radhakrishna N, Mazandarany MP, Hossaini H (2013) Bacterial- aerosol emission from wastewater treatment plant. Desalin Water Treat 51:4478–4488. https://doi.org/10.1080/19443994.2013.769668
Medema G, Wuilings B, Roeleveld P, Van Der Kooij D (2004) Risk assessment of Legionella and enteric pathogens in sewage treatment works. Water Sci Technol Water Supply 4:125–132. https://doi.org/10.2166/ws.2004.0037
Melbostad E, Eduard W, Skogstad A et al (1994) Exposure to bacterial aerosols and work-related symptoms in sewage workers. Am J Ind Med 25:59–63. https://doi.org/10.1002/ajim.4700250116
Ministry of Environmental Protection (2013) Exposure factors handbook of Chinese population. China Environmental Press, Beijing
Mitchell-Blackwood J, Gurian PL, O’Donnell C (2011) Finding risk-based switchover points for response decisions for environmental exposure to Bacillus anthracis. Hum Ecol Risk Assess 17:489–509. https://doi.org/10.1080/10807039.2011.552401
Moran PAP (2012) The dilution assay of viruses. Epidemiol Infect 2:1–52
Pascual L, Pérez-Luz S, Yáñez MA et al (2003) Bioaerosol emission from wastewater treatment plants. Aerobiol (bol) 19:261–270. https://doi.org/10.1023/B:AERO.0000006598.45757.7f
Ramamurthy T, Ghosh A, Pazhani GP, Shinoda S (2014) Current perspectives on viable but non-culturable (VBNC) pathogenic bacteria. Front Public Heal 2:1–9. https://doi.org/10.3389/fpubh.2014.00103
Rasheduzzaman M, Singh R, Haas CN et al (2019) Reverse QMRA as a decision support tool: setting acceptable concentration limits for Pseudomonas aeruginosa and Naegleria fowleri. Water (switzerland) 11:1–15. https://doi.org/10.3390/w11091850
Recer GM, Browne ML, Horn EG et al (2001) Ambient air levels of Aspergillus fumigatus and thermophilic actinomycetes in a residential neighborhood near a yard-waste composting facility. Aerobiol (bol) 17:99–108. https://doi.org/10.1023/A:1010816114787
Regli S, Brose J, Nhaas C, Pgerba C (2018) Modeling the risk from giardia and viruses in drinking water. J Am Water Works Assoc 110:68–72. https://doi.org/10.1002/awwa.1082
Rosenstock L (1995) 42 CFR part 84: respiratory protective devices implications for tuberculosis protection. Infect Control Hosp Epidemiol 16(9):529–531
Rylander R (1999) Health effects among workers in sewage treatment plants. Occup Environ Med 56:354–357. https://doi.org/10.1136/oem.56.5.354
Sales-Ortells H, Agostini G, Medema G (2015) Quantification of waterborne pathogens and associated health risks in urban water. Environ Sci Technol 49:6943–6952. https://doi.org/10.1021/acs.est.5b00625
Sanchez-Monedero MA, Aguilar MI, Fenoll R, Roig A (2008) Effect of the aeration system on the levels of airborne microorganisms generated at wastewater treatment plants. Water Res 42:3739–3744. https://doi.org/10.1016/j.watres.2008.06.028
Shi KW, Wang CW, Jiang SC (2018) Quantitative microbial risk assessment of Greywater on-site reuse. Sci Total Environ 635:1507–1519. https://doi.org/10.1016/j.scitotenv.2018.04.197
Stellacci P, Liberti L, Notarnicola M, Haas CN (2010) Hygienic sustainability of site location of wastewater treatment plants. A case study II Estimating Airborne Biological Hazard. Desalination 253:106–111. https://doi.org/10.1016/j.desal.2009.11.024
Stuart BO (1984) Deposition and clearance of inhaled particles. Environ Health Perspect 55:369–390. https://doi.org/10.1289/ehp.8455369
Szylak-Szydlowski M, Kulig A, Miaśkiewicz-Pęska E (2016) Seasonal changes in the concentrations of airborne bacteria emitted from a large wastewater treatment plant. Int Biodeterior Biodegrad 115:11–16. https://doi.org/10.1016/j.ibiod.2016.07.008
Thorn J, Kerekes E (2001) Health effects among employees in sewage treatment plants: a literature survey. Am J Ind Med 40:170–179. https://doi.org/10.1002/ajim.1085
Travis CC, Morris JM (1992) On the use of 0.75 as an interspecies scaling factor. Risk Anal 12:311–313. https://doi.org/10.1111/j.1539-6924.1992.tb00678.x
Tseng CW, Biancotti JC, Berg BL et al (2015) Increased susceptibility of humanized NSG mice to panton-valentine Leukocidin and Staphylococcus aureus skin infection. PLoS Pathog 11:1–17. https://doi.org/10.1371/journal.ppat.1005292
Upadhyay N, Sun Q, Allen JO et al (2013) Characterization of aerosol emissions from wastewater aeration basins. J Air Waste Manag Assoc 63:20–26. https://doi.org/10.1080/10962247.2012.726693
Wang Y, Lan H, Li L et al (2018a) Chemicals and microbes in bioaerosols from reaction tanks of six wastewater treatment plants: Survival factors, generation sources, and mechanisms. Sci Rep 8:1–12. https://doi.org/10.1038/s41598-018-27652-2
Wang Y, Li L, Han Y et al (2018b) Intestinal bacteria in bioaerosols and factors affecting their survival in two oxidation ditch process municipal wastewater treatment plants located in different regions. Ecotoxicol Environ Saf 154:162–170. https://doi.org/10.1016/j.ecoenv.2018.02.041
Acknowledgements
This study was sponsored by the National Natural Science Foundation of China (51608497) and the Fundamental Research Funds for the Central Universities, China University of Geosciences (Wuhan) (CUGL170409, CUG170103, CUGGC07). We also thank Dr. Zaheer Ahmad Nasir from Cranfield University in UK, Dr. Sonia Garcia-Alcega from The Open University in UK, and Dr. Frederic Coulon from Cranfield University in UK for helping with English writing and editing.
Author information
Authors and Affiliations
Contributions
Cheng Yan and Meng-meng Zhang contributed to conceptualization, methodology, formal analysis and investigation. Cheng Yan, Meng-meng Zhang, and Bei-bei Cui helped in writing—original draft, and writing—review and editing. Cheng Yan contributed to funding acquisition, resources, and supervision.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Editorial responsibility: Agnieszka Galuszka.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yan, C., Zhang, MM. & Cui, BB. Using reverse quantitative microbial risk assessment for estimating acceptable exposure time of bioaerosols in wastewater treatment plants. Int. J. Environ. Sci. Technol. 19, 8713–8726 (2022). https://doi.org/10.1007/s13762-021-03758-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13762-021-03758-5