Spatio-temporal characteristics of genotoxicity in the Yangtze River under the background of COVID-19 pandemic

Highlights

● Genotoxicity was higher in upper Yangtze River than that in the lower reaches.

● COVID-19 changed the seasonal regularity of genotoxicity in lower Yangtze River.

● Water samples exhibited more pronounced genotoxicity compared to sediments.

● Direct genotoxicity being the primary factor and related to antiviral drugs and DBPs.

● 65% or 71% of water posed high or medium risk for Paramecium caudatum or Danio rerio.

Abstract

Abstract The global spread of viruses can lead to the release of large amounts of disinfectants or antiviral drugs into the water environment. The resulting disinfection byproducts (DBPs) and residual antiviral drugs, acting as genotoxic substances or their precursors, may pose risks to aquatic animals and drinking water sources; however, to date, no studies have analyzed the changes in genotoxicity in the Yangtze River before and after the epidemic. In the present study, water and sediment samples from the Yangtze River were collected during different seasons, just before and after the outbreak of COVID-19, and were assessed using the SOS/umu test (with and without liver S9). The results indicated that water samples exhibited more pronounced genotoxicity than did sediments, with direct genotoxicity being the primary factor. Additionally, there were significant regional differences, with notably greater genotoxicity observed in the upper Yangtze River than in the lower reaches before the COVID-19 epidemic. However, this trend was reversed six to ten months later, suggesting the accumulation of DBPs or antiviral drugs after the COVID-19 pandemic. Moreover, the risk quotient indicated that 65% of the water samples posed a high risk for Paramecium caudatum, whereas 71% of the samples posed a medium risk for Danio rerio, thereby representing a potential threat to the ecological security of the Yangtze River. In conclusion, this study, at the basin scale, revealed the impacts of COVID-19 on the Yangtze River, highlighting the need to prevent DBPs and pharmaceutical pollution during similar events in the future.

Graphical abstract

Keywords

Yangtze River / COVID-19 / Genotoxicity / Spatio-temporal characteristics

References

[1] AmésquitaLCruz-BriceñoM NPrieto Z (2018). Damage to human lymphocyte DNA from chloroquine effect. Revista Peruana de Medicina Experimental y Salud Pública, 35(3): 471 (in Spanish)

[2] ArkhipchukV VGarankoN N (2002). A novel nucleolar biomarker in plant and animal cells for assessment of substance cytotoxicity. Environmental Toxicology 17: 187-194

[3] Arvaniti O S, Dasenaki M E, Asimakopoulos A G, Maragou N C, Samaras V G, Antoniou K, Gatidou G, Mamais D, Noutsopoulos C, Frontistis Z. . (2022). Effectiveness of tertiary treatment processes in removing different classes of emerging contaminants from domestic wastewater. Frontiers of Environmental Science & Engineering, 16(11): 148

[4] Beane Freeman L E, Cantor K P, Baris D, Nuckols J R, Johnson A, Colt J S, Schwenn M, Ward M H, Lubin J H, Waddell R. . (2017). Bladder cancer and water disinfection by-product exposures through multiple routes: a population-based case-control study (New England, USA). Environmental Health Perspectives, 125(6): 067010

[5] Chen X, Lei L, Liu S, Han J, Li R, Men J, Li L, Wei L, Sheng Y, Yang L. . (2021). Occurrence and risk assessment of pharmaceuticals and personal care products (PPCPs) against COVID-19 in lakes and WWTP-river-estuary system in Wuhan, China. Science of the Total Environment, 792: 148352

[6] Cui H, Zhu X, Zhu Y, Huang Y, Chen B. (2022). Ecotoxicological effects of DBPs on freshwater phytoplankton communities in co-culture systems. Journal of Hazardous Materials, 421: 126679

[7] de Oliveira L C, de Melo Bisneto A V, Puga S C, Fernandes A S, Véras J H, Cardoso C G, Ribeiro e Silva C, Carneiro C C, Chen Chen L. (2021). Prednisone is genotoxic in mice and Drosophila melanogaster. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 865: 503334

[8] EchigoSItoh SNatsuiTArakiTAndoR (2004). Contribution of brominated organic disinfection by-products to the mutagenicity of drinking water. Water Science and Technology: A Journal of the International Association on Water Pollution Research, 50(5), 321–328

[9] FanY TChang SZhangK FTuXWangS J ZhangM LXie QFuQ (2022). Pollution characteristics and risk assessment of ppcps in typical drinking water sources in the middle reaches of the Yangtze River during the COVID–19 pandemic. Environmental Sciences (Ruse), 43(12): 5522-5533 (in Chinese)

[10] Fang C, Yang X, Ding S, Luan X, Xiao R, Du Z, Wang P, An W, Chu W. (2021). Characterization of dissolved organic matter and its derived disinfection byproduct formation along the Yangtze River. Environmental Science & Technology, 55(18): 12326–12336

[11] FangDYang HZhangHDuHYangJ WeiQ (2022). COVID-19 lockdowns promoted recovery of the Yangtze River’s aquatic ecosystem. Water, 14(22): 3622

[12] Hadj Hassine I, Ben M’hadheb M, Menéndez-Arias L. (2022). Lethal mutagenesis of RNA viruses and approved drugs with antiviral mutagenic activity. Viruses, 14(4): 841

[13] He J, Feng T, Tao L, Peng Y, Tong L, Zhao X, Shao X, Xu L, Yang Y, Zhao Y. (2022). Distribution and impacts on the geological environment of antiviral drugs in major waters of Wuhan, China. China Geology, 5(3): 402–410

[14] Hora P I, Pati S G, McNamara P J, Arnold W A. (2020). Increased use of quaternary ammonium compounds during the SARS-CoV-2 pandemic and beyond: consideration of environmental implications. Environmental Science & Technology Letters, 7(9): 622–631

[15] HuY (2022). Distribution characteristics and ecological risk assessment of PPCPs in surface waters of the Yangtze River. Thesis for the Master Degree. Guilin: Guilin University of Technology (in Chinese)

[16] Huynh N C, Nguyen T T T, Nguyen D T C, Tran T V. (2023). Occurrence, toxicity, impact and removal of selected non-steroidal anti-inflammatory drugs (NSAIDs): a review. Science of the Total Environment, 898: 165317

[17] Jeong C H, Machek E J, Shakeri M, Duirk S E, Ternes T A, Richardson S D, Wagner E D, Plewa M J. (2017). The impact of iodinated X-ray contrast agents on formation and toxicity of disinfection by-products in drinking water. Journal of Environmental Sciences, 58: 173–182

[18] Le Roux J, Plewa M J, Wagner E D, Nihemaiti M, Dad A, Croué J P. (2017). Chloramination of wastewater effluent: toxicity and formation of disinfection byproducts. Journal of Environmental Sciences, 58: 135–145

[19] Liang J, Gao P, Li B, Kang L, Feng L, Han Q, Liu Y, Zhang L. (2022). Characteristics of typical dissolved black carbons and their influence on the formation of disinfection by-products in chlor(am)ination. Frontiers of Environmental Science & Engineering, 16(12): 150

[20] Li J, Wang T, Xue J. (2023). Toxic effects of disinfection by-products on Pseudokirchneriella subcapitata and co-cultured algae community. Science of the Total Environment, 894: 164760

[21] Li Z, Song G, Bi Y, Gao W, He A, Lu Y, Wang Y, Jiang G. (2021). Occurrence and distribution of disinfection byproducts in domestic wastewater effluent, tap water, and surface water during the SARS-CoV-2 pandemic in China. Environmental Science & Technology, 55(7): 4103–4114

[22] Liu J, Hu L, Deng W, Ying G, Hong H, Tsang E P K, Barceló D. (2022). Pilot study of pollution characteristics and ecological risk of disinfection byproducts in natural waters in Hong Kong. Environmental Toxicology and Chemistry, 41(10): 2613–2621

[23] Liu Y H, Zhang S H, Ji G X, Wu S M, Guo R X, Cheng J, Yan Z Y, Chen J Q. (2017). Occurrence, distribution and risk assessment of suspected endocrine-disrupting chemicals in surface water and suspended particulate matter of Yangtze River (Nanjing section). Ecotoxicology and Environmental Safety, 135: 90–97

[24] Marima R, Hull R, Dlamini Z, Penny C. (2020). The dual protease inhibitor lopinavir/ritonavir (LPV/r) exerts genotoxic stress on lung cells. Biomedicine and Pharmacotherapy, 132: 110829

[25] Miyoshi N, Kawano T, Tanaka M, Kadono T, Kosaka T, Kunimoto M, Takahashi T, Hosoya H. (2003). Use of paramecium species in bioassays for environmental risk management: determination of IC50 values for water pollutants. Journal of Health Science, 46: 429–435

[26] Morales-Paredes C A, Rodríguez-Díaz J M, Boluda-Botella N. (2022). Pharmaceutical compounds used in the COVID-19 pandemic: a review of their presence in water and treatment techniques for their elimination. Science of the Total Environment, 814: 152691

[27] Ncube S, Madikizela L M, Chimuka L, Nindi M M. (2018). Environmental fate and ecotoxicological effects of antiretrovirals: a current global status and future perspectives. Water Research, 145: 231–247

[28] Pan Y, Wang Y, Li A, Xu B, Xian Q, Shuang C, Shi P, Zhou Q. (2017). Detection, formation and occurrence of 13 new polar phenolic chlorinated and brominated disinfection byproducts in drinking water. Water Research, 112: 129–136

[29] Postigo C, DeMarini D M, Armstrong M D, Liberatore H K, Lamann K, Kimura S Y, Cuthbertson A A, Warren S H, Richardson S D, McDonald T. . (2018). Chlorination of source water containing iodinated X-ray contrast media: mutagenicity and identification of new iodinated disinfection byproducts. Environmental Science & Technology, 52(22): 13047–13056

[30] Rodriguez Ferreiro G, Cancino Badías L, Lopez-Nigro M, Palermo A, Mudry M, González Elio P, Carballo M A. (2002). DNA single strand breaks in peripheral blood lymphocytes induced by three nitroimidazole derivatives. Toxicology Letters, 132(2): 109–115

[31] Säve-Söderbergh M, Toljander J, Donat-Vargas C, Åkesson A. (2021). Drinking water disinfection by-products and congenital malformations: a nationwide register-based prospective study. Environmental Health Perspectives, 129(9): 097012

[32] Shuliakevich A, Muz M, Oehlmann J, Nagengast L, Schröder K, Wolf Y, Brückner I, Massei R, Brack W, Hollert H, Schiwy S. (2022). Assessing the genotoxic potential of freshwater sediments after extensive rain events – Lessons learned from a case study in an effluent-dominated river in Germany. Water Research, 209: 117921

[33] Sogbanmu T O, Nagy E, Phillips D H, Arlt V M, Otitoloju A A, Bury N R. (2016). Lagos lagoon sediment organic extracts and polycyclic aromatic hydrocarbons induce embryotoxic, teratogenic and genotoxic effects in Danio rerio (zebrafish) embryos. Environmental Science and Pollution Research International, 23(14): 14489–14501

[34] Tang H, Zhong H, Pan Y, Zhou Q, Huo Z, Chu W, Xu B. (2021). A New group of heterocyclic nitrogenous disinfection byproducts (DBPs) in drinking water: role of extraction pH in unknown DBP exploration. Environmental Science & Technology, 55(10): 6764–6772

[35] Wang C, Li Q, Ge F, Hu Z, He P, Chen D, Xu D, Wang P, Zhang Y, Zhang L. . (2022). Responses of aquatic organisms downstream from WWTPs to disinfectants and their by-products during the COVID-19 pandemic, Wuhan. Science of the Total Environment, 818: 151711

[36] WangD (2016). Pollution characteristics and risk of persistent toxic substances from Yangtze River (Yibin to Luzhou) —A case study for heavy metal and polycyclic aromatic hydrocarbons. Thesis for the Master Degree. Handan: Hebei University of Engineering (in Chinese)

[37] Wang L, Zhang X, Chen S, Meng F, Zhang D, Liu Y, Li M, Liu X, Huang X, Qu J. (2021). Spatial variation of dissolved organic nitrogen in Wuhan surface waters: correlation with the occurrence of disinfection byproducts during the COVID-19 pandemic. Water Research, 198: 117138

[38] Wang R, Luo J, Li C, Chen J, Zhu N. (2023). Antiviral drugs in wastewater are on the rise as emerging contaminants: a comprehensive review of spatiotemporal characteristics, removal technologies and environmental risks. Journal of Hazardous Materials, 457: 131694

[39] Waters M D, Warren S, Hughes C, Lewis P, Zhang F. (2022). Human genetic risk of treatment with antiviral nucleoside analog drugs that induce lethal mutagenesis: the special case of molnupiravir. Environmental and Molecular Mutagenesis, 63(1): 37–63

[40] Weil M, Scholz S, Zimmer M, Sacher F, Duis K. (2009). Gene expression analysis in zebrafish embryos: a potential approach to predict effect concentrations in the fish early life stage test. Environmental Toxicology and Chemistry, 28: 1970–1978

[41] Wu Y, Wei W, Luo J, Pan Y, Yang M, Hua M, Chu W, Shuang C, Li A (2022). Comparative toxicity analyses from different endpoints: Are new cyclic disinfection byproducts (DBPs) more toxic than common aliphatic DBPs? Environmental Science & Technology, 56(1): 194–207

[42] XuHLiuY QiWLanH LiuHQuJ LiNLiX MaM (2023). Evaluation of impact of COVID-19 outbreaks on ecotoxicity of surface water in the Yangtze River by luminescent bacteria method. Asian Journal of Ecotoxicology, 18(1): 440-447 (in Chinese)

[43] Xue P, Zhao Y, Zhao D, Chi M, Yin Y, Xuan Y, Wang X. (2021). Mutagenicity, health risk, and disease burden of exposure to organic micropollutants in water from a drinking water treatment plant in the Yangtze River Delta, China. Ecotoxicology and Environmental Safety, 221: 112421

[44] Yan Y, Jiang W W, Li N, Ma M, Wang D H, Wang Z J, Rao K F. (2014). Assessing of genotoxicity of 16 centralized source-waters in China by means of the SOS/umu assay and the micronucleus test: initial identification of the potential genotoxicants by use of a GC/MS method and the QSAR Toolbox 3.0. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 763: 36–43

[45] Yang C, Chen X, Wang H. (2020). Comparisons in concentrations of chlorine compounds in urban section of Nanfeihe River before and after COVID–19 epidemic. Environmental Science & Technology, 43(8): 172–176

[46] ZengCXu HXuYYouSWangX HuYHuangS BianRQi WLanH, . (2021). Distribution and health risk of polycyclic aromatic hydrocarbons (PAHs) and their derivatives in surface water of the Yangtze River. Acta Scientiae Circumstantiae, 41(12): 4932–4941 (in Chinese)

[47] Zhang K F, Chang S, Tu X, Fu Q, Yang G, Fan Y T, Sun X B. (2022). Pollution characteristics and risk assessment of DBPs in typical drinking water sources in Wuhan under the COVID-19 pandemic. Environmental Sciences (Ruse), 43(2): 878–886

[48] Zhang Y, Cheng Z, Xiao F, Wu H, Zou H. (2023). Effects of disinfection by-products in sewage treatment plant effluent on the growth and physiology of Chlorella vulgaris. Environmental Chemistry, 42(2): 370–378

[49] Zhao Z, Gong X, Zhang L, Jin M, Cai Y, Wang X. (2021). Riverine transport and water-sediment exchange of polycyclic aromatic hydrocarbons (PAHs) along the middle-lower Yangtze River, China. Journal of Hazardous Materials, 403: 123973

[50] Zhou X R, Lin Y L, Zhang T Y, Xu B, Chu W H, Cao T C, Zhu W Q. (2019). Speciation and seasonal variation of various disinfection by-products in a full-scale drinking water treatment plant in East China. Water Science and Technology: Water Supply, 19(6): 1579–1586

Acknowledgements

This work was supported by the National Key Research and Development Program (No. 2021YFC3200803), the Scientific Research Project of China Three Gorges Corporation (No. 201903139), the National Key R&D Program of China (No. 2021YFC3200102), the National Natural Science Foundation of China (No. 42007227) and the National Natural Science Foundation of China (No. 52030003), the Natural Science Foundation of Tianjin (No. 22YFYSHZ00060).

Conflict of Interests

The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.

RIGHTS & PERMISSIONS

2024 Higher Education Press 2024