{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T06:52:35Z","timestamp":1791615155318,"version":"4.3.4"},"reference-count":78,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,10,7]],"date-time":"2025-10-07T00:00:00Z","timestamp":1759795200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,10,7]],"date-time":"2025-10-07T00:00:00Z","timestamp":1759795200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100009367","name":"Mansoura University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100009367","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:p>Fish and their ectoparasites serve as model organisms for evaluating aquatic ecosystem health and can thus function as bioindicators of environmental pollution. This study, therefore, investigates the gene expression of biomarkers of effect in <jats:italic>Clarias gariepinus<\/jats:italic> inhabiting a polluted drain called the Kitchener Drain and the Nile River (a reference habitat). Ectoparasites and metacercariae of digenean endoparasites on the collected fish were examined to further clarify the impact of pollution. Compared with the Nile River, the Kitchener Drain contained significantly elevated concentrations of heavy metals, bicarbonates, sulfates, and minerals. Interestingly, the prevalence, mean intensity, and abundance of ectoparasitic monogeneans from <jats:italic>C. gariepinus<\/jats:italic> collected from the Nile River were higher compared with those from the Kitchener Drain, whereas the drain had higher levels of metacercaria of the digenean endoparasite <jats:italic>Centrocestus formosanus<\/jats:italic>. Fish from the Kitchener Drain had significantly elevated hepatic expressions of genes related to metal toxicity, oxidative stress, inflammation, heat shock response, and xenobiotic metabolism. The results indicate that <jats:italic>C. gariepinus<\/jats:italic> exposed to metals and other pollutants triggers an adaptive response involving multiple stress-response pathways. The findings also highlight the impact of pollution on parasitic infestation in this fish population. The study supports the utilization of molecular biomarkers and ectoparasitic infestation as early warning signals for water pollution.<\/jats:p>","DOI":"10.1038\/s41598-025-20433-8","type":"journal-article","created":{"date-parts":[[2025,10,7]],"date-time":"2025-10-07T19:40:24Z","timestamp":1759866024000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Integrating molecular biomarkers and ectoparasitic infestation to assess water quality"],"prefix":"10.1038","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3057-6698","authenticated-orcid":false,"given":"Hamada S.","family":"Salem","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rana H.","family":"Omar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ahmed M.","family":"El-Naggar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amira A.","family":"Ibrahim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9053-5014","authenticated-orcid":false,"given":"Mohamed I.","family":"Mashaly","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,10,7]]},"reference":[{"key":"20433_CR1","doi-asserted-by":"publisher","first-page":"103173","DOI":"10.1016\/j.rsma.2023.103173","volume":"66","author":"AA Metwally","year":"2023","unstructured":"Metwally, A. A., Khalafallah, M. M. & Dawood, M. A. O. Assessment of the water quality, the human health risk, and heavy metal accumulation in nile tilapia and African catfish collected from the Kitchener Drain-Egypt. Reg. Stud. Mar. Sci. 66, 103173. https:\/\/doi.org\/10.1016\/j.rsma.2023.103173 (2023).","journal-title":"Reg. Stud. Mar. Sci."},{"key":"20433_CR2","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1016\/j.molliq.2017.05.063","volume":"240","author":"I Anastopoulos","year":"2017","unstructured":"Anastopoulos, I., Bhatnagar, A., Hameed, B. H., Ok, Y. S. & Omirou, M. A review on waste-derived adsorbents from sugar industry for pollutant removal in water and wastewater. J. Mol. Liq. 240, 179\u2013188. https:\/\/doi.org\/10.1016\/j.molliq.2017.05.063 (2017).","journal-title":"J. Mol. Liq"},{"key":"20433_CR3","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1186\/s12302-020-00316-7","volume":"32","author":"D Tenji","year":"2020","unstructured":"Tenji, D. et al. Fish biomarkers from a different perspective: evidence of adaptive strategy of Abramis Brama (L.) to chemical stress. Environ. Sci. Eur. 32, 47. https:\/\/doi.org\/10.1186\/s12302-020-00316-7 (2020).","journal-title":"Environ. Sci. Eur."},{"key":"20433_CR4","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1007\/s00128-021-03341-1","volume":"107","author":"HS Salem","year":"2021","unstructured":"Salem, H. S., Hagras, A. E., El-Baghdady, H. A. M. & El-Naggar, A. M. Biomarkers of exposure and effect in nile tilapia (Oreochromis niloticus) environmentally exposed to multiple stressors in Egypt. Bull. Environ. Contam. Toxicol. 107, 889\u2013894. https:\/\/doi.org\/10.1007\/s00128-021-03341-1 (2021).","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"20433_CR5","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.cbpc.2018.10.002","volume":"215","author":"R Jia","year":"2019","unstructured":"Jia, R. et al. Antioxidative, anti-inflammatory and hepatoprotective effects of Resveratrol on oxidative stress-induced liver damage in tilapia (Oreochromis niloticus). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 215, 56\u201366. https:\/\/doi.org\/10.1016\/j.cbpc.2018.10.002 (2019).","journal-title":"Comp. Biochem. Physiol. C Toxicol. Pharmacol."},{"key":"20433_CR6","doi-asserted-by":"publisher","first-page":"198","DOI":"10.3923\/ijzr.2015.198.206","volume":"11","author":"EM Bayoumy","year":"2015","unstructured":"Bayoumy, E. M., Abou-El-dobal, S. K. A. & Hassanain, M. A. Assessment of heavy metal pollution and fish parasites as biological indicators at Arabian Gulf off Dammam Coast, Saudi Arabia. Int. J. Zool. Res. 11, 198\u2013206. https:\/\/doi.org\/10.3923\/ijzr.2015.198.206 (2015).","journal-title":"Int. J. Zool. Res."},{"key":"20433_CR7","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1017\/S0022149X09990563","volume":"84","author":"G Madanire-Moyo","year":"2010","unstructured":"Madanire-Moyo, G. & Barson, M. Diversity of metazoan parasites of the African catfish Clarias Gariepinus (Burchell, 1822) as indicators of pollution in a subtropical African river system. J. Helminthol. 84, 216\u2013227. https:\/\/doi.org\/10.1017\/S0022149X09990563 (2010).","journal-title":"J. Helminthol"},{"key":"20433_CR8","doi-asserted-by":"publisher","first-page":"E1","DOI":"10.4102\/ojvr.v79i1.362","volume":"79","author":"GN Madanire-Moyo","year":"2012","unstructured":"Madanire-Moyo, G. N., Luus-Powell, W. J. & Olivier, P. A. Diversity of metazoan parasites of the Mozambique tilapia, Oreochromis mossambicus (Peters, 1852), as indicators of pollution in the Limpopo and olifants river systems. Onderstepoort J. Vet. Res. 79, E1\u20139. https:\/\/doi.org\/10.4102\/ojvr.v79i1.362 (2012).","journal-title":"Onderstepoort J. Vet. Res."},{"key":"20433_CR9","doi-asserted-by":"publisher","first-page":"7762","DOI":"10.1038\/s41598-024-57036-8","volume":"14","author":"M Shehata","year":"2024","unstructured":"Shehata, M. et al. Integrated management of groundwater quantity, physicochemical properties, and microbial quality in West nile delta using a new MATLAB code and geographic information system mapping. Sci. Rep. 14, 7762. https:\/\/doi.org\/10.1038\/s41598-024-57036-8 (2024).","journal-title":"Sci. Rep."},{"key":"20433_CR10","unstructured":"American Public Health Association. Standard Methods for the Examination of Water and Wastewater, 23rd edn. (American Public Health Association, 2017)."},{"key":"20433_CR11","doi-asserted-by":"publisher","first-page":"e0191314","DOI":"10.1371\/journal.pone.0191314","volume":"13","author":"T Nasrabadi","year":"2018","unstructured":"Nasrabadi, T. et al. Bulk metal concentrations versus total suspended solids in rivers: Time-invariant & catchment-specific relationships. PLoS One. 13, e0191314. https:\/\/doi.org\/10.1371\/journal.pone.0191314 (2018).","journal-title":"PLoS One"},{"key":"20433_CR12","unstructured":"International Organization for Standardization. Water quality\u2014Determination of Selected Elements by Inductively Coupled Plasma Optical Emission Spectrometry (ICPOES); ISO 11885:2007 (International Organization for Standardization, 2007)."},{"key":"20433_CR13","unstructured":"Mindak, W. R., Cheng, J., Hight, S. C. & Capar, S. G. Elemental Analysis Manual (US Food and Drug Administration, 2014)."},{"key":"20433_CR14","unstructured":"Canadian Council of Ministers of the Environment. Canadian Water Quality Guidelines for the Protection of Aquatic Life (Canadian Council of Ministers of the Environment, 2017)."},{"key":"20433_CR15","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.ejar.2016.12.006","volume":"43","author":"AM Abdel-Satar","year":"2017","unstructured":"Abdel-Satar, A. M., Ali, M. H. & Goher, M. E. Indices of water quality and metal pollution of nile River, Egypt. Egypt J. Aquat. Res. 43, 21\u201329. https:\/\/doi.org\/10.1016\/j.ejar.2016.12.006 (2017).","journal-title":"Egypt J. Aquat. Res."},{"key":"20433_CR16","unstructured":"Egyptian Ministry of Health. Egyptian Drinking Water Quality standards. Population Decision Number 458 (Egyptian Ministry of Health, 2007)."},{"key":"20433_CR17","unstructured":"World Health Organization. Guidelines for drinking-water Quality 4th edn (World Health Organization, 2022)."},{"key":"20433_CR18","unstructured":"Ayers, R. S. & Westcot, D. W. Water Quality for AgricultureVol. 29 (Food and Agriculture Organization of the United Nations, 1985)."},{"key":"20433_CR19","doi-asserted-by":"publisher","unstructured":"Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402\u2013408 (2001). https:\/\/doi.org\/10.1006\/meth.2001.1262","DOI":"10.1006\/meth.2001.1262"},{"key":"20433_CR20","first-page":"14","volume":"13","author":"I Paperna","year":"1961","unstructured":"Paperna, I. Studies on monogenetic trematodes in Israel. 3. Monogenetic trematodes of the Cyprinidae and claridae of the lake of galilee. Bamidgeh 13, 14\u201329 (1961).","journal-title":"Bamidgeh"},{"key":"20433_CR21","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1007\/bf00009869","volume":"8","author":"MM El-Naggar","year":"1986","unstructured":"El-Naggar, M. M. & Serag, H. M. Quadriacanthus aegypticus n. sp., a monogenean gill parasite from the Egyptian teleost Clarias lazera. Syst. Parasitol. 8, 129\u2013140. https:\/\/doi.org\/10.1007\/bf00009869 (1986).","journal-title":"Syst. Parasitol."},{"key":"20433_CR22","first-page":"77","volume":"87","author":"R Ergens","year":"1973","unstructured":"Ergens, R. Two new species of Gyrodactylus from Clarias lazera (Vermes, Trematoda, Monogenoidea). Rev. Zool. Bot. Afric. 87, 77\u201380 (1973).","journal-title":"Rev. Zool. Bot. Afric"},{"key":"20433_CR23","first-page":"490","volume":"136","author":"A Gussev","year":"1961","unstructured":"Gussev, A. A viviparous monogenetic trematode from freshwater basins of Africa. Dokl. Akad. Nauk. SSSR. 136, 490\u2013493 (1961).","journal-title":"Dokl. Akad. Nauk. SSSR"},{"key":"20433_CR24","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.exppara.2016.06.007","volume":"168","author":"F Yousif","year":"2016","unstructured":"Yousif, F., Ayoub, M., Tadros, M. & El Bardicy The first record of centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Egypt. Exp. Parasitol. 168, 56\u201361. https:\/\/doi.org\/10.1016\/j.exppara.2016.06.007 (2016).","journal-title":"Exp. Parasitol."},{"key":"20433_CR25","doi-asserted-by":"publisher","unstructured":"Bush, A. O., Lafferty, K. D., Lotz, J. M. & Shostak, A. W. Parasitology Meets ecology on its own terms: Margolis et al. Revisited. J. Parasitol. 83 https:\/\/doi.org\/10.2307\/3284227 (1997).","DOI":"10.2307\/3284227"},{"key":"20433_CR26","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1645\/0022-3395(2000)086","volume":"86","author":"L R\u00f3zsa","year":"2000","unstructured":"R\u00f3zsa, L., Reiczigel, J. & Majoros, G. Quantifying parasites in samples of hosts. J. Parasitol. 86, 228\u2013232. https:\/\/doi.org\/10.1645\/0022-3395(2000)086 (2000). [0228:Qpisoh]2.0.Co;2.","journal-title":"J. Parasitol."},{"key":"20433_CR27","doi-asserted-by":"publisher","unstructured":"Ameen, M. M., Darwish, D. H., Salama, A. M., Serag, M. S. & Beheary, M. S. Water quality and bacteriological assessment of two drains; in the deltaic mediterranean Coast of Egypt. Egypt. J. Aquat. Biol. Fish. 27 https:\/\/doi.org\/10.21608\/ejabf.2023.327965 (2023).","DOI":"10.21608\/ejabf.2023.327965"},{"key":"20433_CR28","doi-asserted-by":"publisher","first-page":"4089","DOI":"10.1007\/s10653-021-00893-3","volume":"43","author":"MA Abdelhafiz","year":"2021","unstructured":"Abdelhafiz, M. A. et al. Chemical and bacterial quality monitoring of the nile river water and associated health risks in Qena-Sohag sector, Egypt. Environ. Geochem. Health. 43, 4089\u20134104. https:\/\/doi.org\/10.1007\/s10653-021-00893-3 (2021).","journal-title":"Environ. Geochem. Health"},{"key":"20433_CR29","doi-asserted-by":"publisher","first-page":"9734","DOI":"10.1038\/s41598-020-66757-5","volume":"10","author":"D Qi","year":"2020","unstructured":"Qi, D., Wu, Q. & Zhu, J. Nitrogen and phosphorus losses from paddy fields and the yield of rice with different water and nitrogen management practices. Sci. Rep. 10, 9734. https:\/\/doi.org\/10.1038\/s41598-020-66757-5 (2020).","journal-title":"Sci. Rep."},{"key":"20433_CR30","doi-asserted-by":"publisher","first-page":"2480","DOI":"10.1038\/s41598-019-38481-2","volume":"9","author":"J Lu","year":"2019","unstructured":"Lu, J., Zhu, B., Struewing, I., Xu, N. & Duan, S. Nitrogen-phosphorus-associated metabolic activities during the development of a cyanobacterial bloom revealed by metatranscriptomics. Sci. Rep. 9, 2480. https:\/\/doi.org\/10.1038\/s41598-019-38481-2 (2019).","journal-title":"Sci. Rep."},{"key":"20433_CR31","doi-asserted-by":"publisher","first-page":"85","DOI":"10.3390\/soilsystems7040085","volume":"7","author":"YA El-Amier","year":"2023","unstructured":"El-Amier, Y. A., Bonanomi, G. & Abd-ElGawad, A. M. Pollution risk assessment of heavy metals along Kitchener drain sediment, nile delta. Soil. Syst. 7, 85. https:\/\/doi.org\/10.3390\/soilsystems7040085 (2023).","journal-title":"Soil. Syst."},{"key":"20433_CR32","doi-asserted-by":"publisher","first-page":"3981","DOI":"10.3390\/w14233981","volume":"14","author":"A Abdelaal","year":"2022","unstructured":"Abdelaal, A., Abdelkader, A. I., Alshehri, F., Elatiar, A. & Almadani, S. A. Assessment and Spatiotemporal variability of heavy metals pollution in water and sediments of a coastal landscape at the nile delta. Water 14, 3981. https:\/\/doi.org\/10.3390\/w14233981 (2022).","journal-title":"Water"},{"key":"20433_CR33","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1007\/s10661-024-12541-1","volume":"196","author":"F Ramadan","year":"2024","unstructured":"Ramadan, F. et al. Heavy metal contamination and environmental risk assessment: a case study of surface water in the Bahr mouse stream, East nile Delta, Egypt. Environ. Monit. Assess. 196, 429. https:\/\/doi.org\/10.1007\/s10661-024-12541-1 (2024).","journal-title":"Environ. Monit. Assess."},{"key":"20433_CR34","doi-asserted-by":"publisher","unstructured":"Al-Afify, A. D. G. & Abdel-Satar, A. M. Heavy metal contamination of the river nile environment, Rosetta Branch, Egypt. Water Air Soil. Pollut. 233 https:\/\/doi.org\/10.1007\/s11270-022-05759-7 (2022).","DOI":"10.1007\/s11270-022-05759-7"},{"key":"20433_CR35","doi-asserted-by":"publisher","unstructured":"Shetaia, S. A., Elhebiry, M. S., Ashry, E., Mohsen, M. & M. & Distribution and ecological health risk assessment of heavy metals in Damietta branch of nile River, Egypt. Int. J. River Basin Manag. 1\u201312. https:\/\/doi.org\/10.1080\/15715124.2024.2390562 (2024).","DOI":"10.1080\/15715124.2024.2390562"},{"key":"20433_CR36","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.chemosphere.2014.01.030","volume":"108","author":"DK Gupta","year":"2014","unstructured":"Gupta, D. K., Chatterjee, S., Datta, S., Veer, V. & Walther, C. Role of phosphate fertilizers in heavy metal uptake and detoxification of toxic metals. Chemosphere 108, 134\u2013144. https:\/\/doi.org\/10.1016\/j.chemosphere.2014.01.030 (2014).","journal-title":"Chemosphere"},{"key":"20433_CR37","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.3390\/w14071131","volume":"14","author":"M Gad","year":"2022","unstructured":"Gad, M., Saleh, A. H., Hussein, H., Farouk, M. & Elsayed, S. Appraisal of surface water quality of nile river using water quality indices, spectral signature and multivariate modeling. Water 14, 1131. https:\/\/doi.org\/10.3390\/w14071131 (2022).","journal-title":"Water"},{"key":"20433_CR38","doi-asserted-by":"publisher","first-page":"801","DOI":"10.21608\/ajs.2021.55062.1320","volume":"29","author":"E Abd-Elfattah","year":"2021","unstructured":"Abd-Elfattah, E., Sheta, A. E. A., Saifeldeen, M., Hassanein, S. & Mahmoud, Y. Assessment of water and sediments quality of Kitchener drain, nile Delta, Egypt. Arab. Univ. J. Agric. Sci. 29, 801\u2013811. https:\/\/doi.org\/10.21608\/ajs.2021.55062.1320 (2021).","journal-title":"Arab. Univ. J. Agric. Sci."},{"key":"20433_CR39","doi-asserted-by":"publisher","first-page":"378","DOI":"10.21608\/ajbas.2022.169528.1130","volume":"4","author":"A Elatiar","year":"2022","unstructured":"Elatiar, A., Abdelkader, A. & Abdelaal, A. Assessment of water quality and bacteriological indicators of sewage pollution in Bahr El-Baqar Drain, Eastern nile Delta, Egypt. Alfarama J. Basic. Appl. Sci. 4, 378\u2013390. https:\/\/doi.org\/10.21608\/ajbas.2022.169528.1130 (2022).","journal-title":"Alfarama J. Basic. Appl. Sci."},{"key":"20433_CR40","doi-asserted-by":"publisher","first-page":"1129","DOI":"10.21608\/ejabf.2024.361963","volume":"28","author":"AS Eldourghamy","year":"2024","unstructured":"Eldourghamy, A. S., Goher, M. E., Hagag, Y. M. & Rizk, N. M. H. Assessment of the water quality in the Damietta branch of the nile River, Egypt. Egypt. J. Aquat. Biol. Fish. 28, 1129\u20131157 (2024).","journal-title":"Egypt. J. Aquat. Biol. Fish."},{"key":"20433_CR41","doi-asserted-by":"publisher","first-page":"18","DOI":"10.3390\/antiox13010018","volume":"13","author":"S Parida","year":"2023","unstructured":"Parida, S. & Sahoo, P. K. Antioxidant defence in Labeo Rohita to biotic and abiotic stress: insight from mRNA expression, molecular characterization and Recombinant protein-based ELISA of catalase, glutathione peroxidase, CuZn superoxide dismutase, and glutathione S-transferase. Antioxid. (Basel). 13, 18. https:\/\/doi.org\/10.3390\/antiox13010018 (2023).","journal-title":"Antioxid. (Basel)"},{"key":"20433_CR42","doi-asserted-by":"publisher","first-page":"126630","DOI":"10.1016\/j.chemosphere.2020.126630","volume":"253","author":"OR Ibor","year":"2020","unstructured":"Ibor, O. R. et al. Biotransformation and oxidative stress responses in relation to tissue contaminant burden in Clarias Gariepinus exposed to simulated leachate from a solid waste dumpsite in Calabar, Nigeria. Chemosphere 253, 126630. https:\/\/doi.org\/10.1016\/j.chemosphere.2020.126630 (2020).","journal-title":"Chemosphere"},{"key":"20433_CR43","doi-asserted-by":"publisher","first-page":"596","DOI":"10.1577\/1548-8659(1986)115<596:MIF>2.0.CO;2","volume":"115","author":"SJ Hamilton","year":"1986","unstructured":"Hamilton, S. J. & Mehrle, P. M. Metallothionein in fish: review of its importance in assessing stress from metal contaminants. Trans. Am. Fish. Soc. 115, 596\u2013609. https:\/\/doi.org\/10.1577\/1548-8659(1986)115%3C596:MIF%3E2.0.CO;2 (1986).","journal-title":"Trans. Am. Fish. Soc."},{"key":"20433_CR44","doi-asserted-by":"publisher","first-page":"513","DOI":"10.1007\/s12210-022-01092-7","volume":"33","author":"A Monjane-Mabuie","year":"2022","unstructured":"Monjane-Mabuie, A., Mondlane-Milisse, A., Pedro, O., Le\u00e3o-Buchir, J. & Correia, D. Mercury pollution assessment and Metallothionein gene expression in tilapia (Oreochromis mossambicus): a case study of Revu\u00e8 river in Manica, Mozambique. Rend. Lincei Sci. Fis. Nat. 33, 513\u2013526. https:\/\/doi.org\/10.1007\/s12210-022-01092-7 (2022).","journal-title":"Rend. Lincei Sci. Fis. Nat."},{"key":"20433_CR45","doi-asserted-by":"publisher","first-page":"114693","DOI":"10.1016\/j.envpol.2020.114693","volume":"264","author":"SB Swaleh","year":"2020","unstructured":"Swaleh, S. B., Banday, U. Z., Asadi, M. A. & Usmani, N. Biochemical profile and gene expression of Clarias Gariepinus as a signature of heavy metal stress. Environ. Pollut. 264, 114693. https:\/\/doi.org\/10.1016\/j.envpol.2020.114693 (2020).","journal-title":"Environ. Pollut"},{"key":"20433_CR46","doi-asserted-by":"publisher","first-page":"5154","DOI":"10.1021\/es070455p","volume":"41","author":"L Quiros","year":"2007","unstructured":"Quiros, L. et al. Physiological response to persistent organic pollutants in fish from mountain lakes: analysis of CYP1A gene expression in natural populations of Salmo trutta. Environ. Sci. Technol. 41, 5154\u20135160. https:\/\/doi.org\/10.1021\/es070455p (2007).","journal-title":"Environ. Sci. Technol."},{"key":"20433_CR47","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.ecoenv.2013.07.029","volume":"98","author":"S Rajeshkumar","year":"2013","unstructured":"Rajeshkumar, S., Mini, J. & Munuswamy, N. Effects of heavy metals on antioxidants and expression of HSP70 in different tissues of milk fish (Chanos chanos) of Kaattuppalli Island, Chennai, India. Ecotoxicol. Environ. Saf. 98, 8\u201318. https:\/\/doi.org\/10.1016\/j.ecoenv.2013.07.029 (2013).","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"20433_CR48","doi-asserted-by":"publisher","first-page":"643","DOI":"10.1007\/s13762-023-04971-0","volume":"21","author":"B Rangaswamy","year":"2023","unstructured":"Rangaswamy, B., Kim, W. S. & Kwak, I. S. Heat shock protein 70 reflected the state of inhabited fish response to water quality within lake ecosystem. Int. J. Environ. Sci. Technol. (Tehran). 21, 643\u2013654. https:\/\/doi.org\/10.1007\/s13762-023-04971-0 (2023).","journal-title":"Int. J. Environ. Sci. Technol. (Tehran)"},{"key":"20433_CR49","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.cytogfr.2011.10.001","volume":"22","author":"G Lopez-Castejon","year":"2011","unstructured":"Lopez-Castejon, G. & Brough, D. Understanding the mechanism of IL-1beta secretion. Cytokine Growth Factor. Rev. 22, 189\u2013195. https:\/\/doi.org\/10.1016\/j.cytogfr.2011.10.001 (2011).","journal-title":"Cytokine Growth Factor. Rev."},{"key":"20433_CR50","doi-asserted-by":"publisher","first-page":"72","DOI":"10.3390\/toxics9040072","volume":"9","author":"SP Shetty","year":"2021","unstructured":"Shetty, S. P. Inflammatory biomarkers Interleukin 1 beta (IL-1beta) and tumour necrosis factor alpha (TNF-alpha) are differentially elevated in tobacco smoke associated COPD and biomass smoke associated COPD. Toxics 9, 72. https:\/\/doi.org\/10.3390\/toxics9040072 (2021).","journal-title":"Toxics"},{"key":"20433_CR51","doi-asserted-by":"publisher","first-page":"155828","DOI":"10.1016\/j.cyto.2022.155828","volume":"153","author":"K Matsushima","year":"2022","unstructured":"Matsushima, K., Yang, D. & Oppenheim, J. J. Interleukin-8: an evolving chemokine. Cytokine 153, 155828. https:\/\/doi.org\/10.1016\/j.cyto.2022.155828 (2022).","journal-title":"Cytokine"},{"key":"20433_CR52","doi-asserted-by":"publisher","first-page":"17023","DOI":"10.1038\/sigtrans.2017.23","volume":"2","author":"T Liu","year":"2017","unstructured":"Liu, T., Zhang, L., Joo, D. & Sun, S. C. NF-kappaB signaling in inflammation. Signal. Transduct. Target. Ther. 2, 17023. https:\/\/doi.org\/10.1038\/sigtrans.2017.23 (2017).","journal-title":"Signal. Transduct. Target. Ther."},{"key":"20433_CR53","doi-asserted-by":"publisher","first-page":"8361","DOI":"10.3390\/ijerph18168361","volume":"18","author":"M Kulasza","year":"2021","unstructured":"Kulasza, M. & Skuza, L. Changes of gene expression patterns from aquatic organisms exposed to metal nanoparticles. Int. J. Environ. Res. Public. Health. 18, 8361. https:\/\/doi.org\/10.3390\/ijerph18168361 (2021).","journal-title":"Int. J. Environ. Res. Public. Health"},{"key":"20433_CR54","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.cbpc.2019.04.012","volume":"222","author":"D Xie","year":"2019","unstructured":"Xie, D., Li, Y., Liu, Z. & Chen, Q. Inhibitory effect of cadmium exposure on digestive activity, antioxidant capacity and immune defense in the intestine of yellow catfish (Pelteobagrus fulvidraco). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 222, 65\u201373. https:\/\/doi.org\/10.1016\/j.cbpc.2019.04.012 (2019).","journal-title":"Comp. Biochem. Physiol. C Toxicol. Pharmacol."},{"key":"20433_CR55","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/j.fsi.2017.10.047","volume":"72","author":"J Yin","year":"2018","unstructured":"Yin, J. et al. Time-response characteristic and potential biomarker identification of heavy metal induced toxicity in zebrafish. Fish. Shellfish Immunol. 72, 309\u2013317. https:\/\/doi.org\/10.1016\/j.fsi.2017.10.047 (2018).","journal-title":"Fish. Shellfish Immunol."},{"key":"20433_CR56","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.aquatox.2016.09.012","volume":"180","author":"JL Zheng","year":"2016","unstructured":"Zheng, J. L., Yuan, S. S., Wu, C. W. & Lv, Z. M. Acute exposure to waterborne cadmium induced oxidative stress and immunotoxicity in the brain, ovary and liver of zebrafish (Danio rerio). Aquat. Toxicol. 180, 36\u201344. https:\/\/doi.org\/10.1016\/j.aquatox.2016.09.012 (2016).","journal-title":"Aquat. Toxicol."},{"key":"20433_CR57","doi-asserted-by":"publisher","first-page":"219","DOI":"10.22102\/jaehr.2016.45840","volume":"4","author":"J Biswas","year":"2016","unstructured":"Biswas, J. & Pramanik, S. Assessment of aquatic environmental quality using gyrodactylus sp. as a living probe: parasitic biomonitoring of ecosystem health. J. Adv. Environ. Health Res. 4, 219\u2013226. https:\/\/doi.org\/10.22102\/jaehr.2016.45840 (2016).","journal-title":"J. Adv. Environ. Health Res."},{"key":"20433_CR58","doi-asserted-by":"publisher","first-page":"114268","DOI":"10.1016\/j.marpolbul.2022.114268","volume":"185","author":"H Sue","year":"2022","unstructured":"Sue, H., MacKenzie, K., Ives, S. C., Pert, C. C. & Jones, C. S. Diclidophora Merlangi (Kuhn, 1829) Kroyer, 1838 (Monogenea: Diclidophoridae) as an indicator of hydrocarbon pollution in the North sea. Mar. Pollut Bull. 185, 114268. https:\/\/doi.org\/10.1016\/j.marpolbul.2022.114268 (2022).","journal-title":"Mar. Pollut Bull."},{"key":"20433_CR59","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.1645\/GE-1162R.1","volume":"93","author":"C Sanchez-Ramirez","year":"2007","unstructured":"Sanchez-Ramirez, C. et al. Cichlidogyrus sclerosus (Monogenea: Ancyrocephalinae) and its host, the nile tilapia (Oreochromis niloticus), as bioindicators of chemical pollution. J. Parasitol. 93, 1097\u20131106. https:\/\/doi.org\/10.1645\/GE-1162R.1 (2007).","journal-title":"J. Parasitol."},{"key":"20433_CR60","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1007\/s10452-019-09676-6","volume":"53","author":"JM Falkenberg","year":"2019","unstructured":"Falkenberg, J. M. et al. Gill parasites of fish and their relation to host and environmental factors in two estuaries in Northeastern Brazil. Aquat. Ecol. 53, 109\u2013118. https:\/\/doi.org\/10.1007\/s10452-019-09676-6 (2019).","journal-title":"Aquat. Ecol."},{"key":"20433_CR61","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1186\/s13071-017-2001-3","volume":"10","author":"B Sures","year":"2017","unstructured":"Sures, B., Nachev, M., Selbach, C. & Marcogliese, D. J. Parasite responses to pollution: what we know and where we go in \u2018environmental parasitology\u2019. Parasit. Vectors. 10, 65. https:\/\/doi.org\/10.1186\/s13071-017-2001-3 (2017).","journal-title":"Parasit. Vectors"},{"key":"20433_CR62","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.aquatox.2009.03.002","volume":"93","author":"CA Blanar","year":"2009","unstructured":"Blanar, C. A., Munkittrick, K. R., Houlahan, J., Maclatchy, D. L. & Marcogliese, D. J. Pollution and parasitism in aquatic animals: a meta-analysis of effect size. Aquat. Toxicol. 93, 18\u201328. https:\/\/doi.org\/10.1016\/j.aquatox.2009.03.002 (2009).","journal-title":"Aquat. Toxicol."},{"key":"20433_CR63","doi-asserted-by":"publisher","first-page":"108062","DOI":"10.1016\/j.ecolind.2021.108062","volume":"130","author":"BM Gilbert","year":"2021","unstructured":"Gilbert, B. M. & Avenant-Oldewage, A. Monogeneans as bioindicators: A meta-analysis of effect size of contaminant exposure toward monogenea (Platyhelminthes). Ecol. Indic. 130, 108062. https:\/\/doi.org\/10.1016\/j.ecolind.2021.108062 (2021).","journal-title":"Ecol. Indic."},{"key":"20433_CR64","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/B978-0-12-398457-9.00002-4","volume":"79","author":"NJ Morley","year":"2012","unstructured":"Morley, N. J. Thermodependent helminth infections: the influence of climate change on parasitic diseases. Adv. Parasitol. 79, 99\u2013167. https:\/\/doi.org\/10.1016\/B978-0-12-398457-9.00002-4 (2012).","journal-title":"Adv. Parasitol."},{"key":"20433_CR65","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1016\/j.pt.2004.01.014","volume":"20","author":"B Sures","year":"2004","unstructured":"Sures, B. Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends Parasitol. 20, 170\u2013177. https:\/\/doi.org\/10.1016\/j.pt.2004.01.014 (2004).","journal-title":"Trends Parasitol."},{"key":"20433_CR66","doi-asserted-by":"publisher","first-page":"925","DOI":"10.4319\/lo.1999.44.3_part_2.0925","volume":"44","author":"KD Lafferty","year":"1999","unstructured":"Lafferty, K. D. & Kuris, A. M. How environmental stress affects the impacts of parasites. Limnol. Oceanogr. 44, 925\u2013931. https:\/\/doi.org\/10.4319\/lo.1999.44.3_part_2.0925 (1999).","journal-title":"Limnol. Oceanogr."},{"key":"20433_CR67","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.pt.2009.11.001","volume":"26","author":"VM Vidal-Martinez","year":"2010","unstructured":"Vidal-Martinez, V. M., Pech, D., Sures, B., Purucker, S. T. & Poulin, R. Can parasites really reveal environmental impact? Trends Parasitol. 26, 44\u201351. https:\/\/doi.org\/10.1016\/j.pt.2009.11.001 (2010).","journal-title":"Trends Parasitol."},{"key":"20433_CR68","doi-asserted-by":"publisher","unstructured":"Shuhaimi-Othman, M., Nur-Amalina, R. & Nadzifah, Y. Toxicity of metals to a freshwater snail, Melanoides tuberculata. ScientificWorldJournal\u00a02012,\u00a0125785 (2012).\u00a0https:\/\/doi.org\/10.1100\/2012\/125785","DOI":"10.1100\/2012\/125785"},{"key":"20433_CR69","doi-asserted-by":"publisher","first-page":"839746","DOI":"10.3389\/fimmu.2022.839746","volume":"13","author":"AE Lynch","year":"2022","unstructured":"Lynch, A. E., Noble, L. R., Jones, C. S. & Routledge, E. J. Common aquatic pollutants modify hemocyte immune responses in biomphalaria glabrata. Front. Immunol. 13, 839746. https:\/\/doi.org\/10.3389\/fimmu.2022.839746 (2022).","journal-title":"Front. Immunol."},{"key":"20433_CR70","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1016\/j.exppara.2008.12.001","volume":"121","author":"MFM Soliman","year":"2009","unstructured":"Soliman, M. F. M. Fasciola gigantica: cercarial shedding pattern from lymnaea natalensis after long-term exposure to cadmium at different temperatures. Exp. Parasitol. 121, 307\u2013311. https:\/\/doi.org\/10.1016\/j.exppara.2008.12.001 (2009).","journal-title":"Exp. Parasitol."},{"key":"20433_CR71","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1016\/s0065-308x(08)60070-6","volume":"35","author":"K MacKenzie","year":"1995","unstructured":"MacKenzie, K., Williams, H. H., Williams, B., McVicar, A. H. & Siddall, R. Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv. Parasitol. 35, 85\u2013144. https:\/\/doi.org\/10.1016\/s0065-308x(08)60070-6 (1995).","journal-title":"Adv. Parasitol."},{"key":"20433_CR72","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/s1383-5769(02)00008-9","volume":"51","author":"JY Chai","year":"2002","unstructured":"Chai, J. Y. & Lee, S. H. Food-borne intestinal trematode infections in the Republic of Korea. Parasitol. Int. 51, 129\u2013154. https:\/\/doi.org\/10.1016\/s1383-5769(02)00008-9 (2002).","journal-title":"Parasitol. Int."},{"key":"20433_CR73","doi-asserted-by":"publisher","first-page":"737418","DOI":"10.1016\/j.aquaculture.2021.737418","volume":"546","author":"ZA Kari","year":"2022","unstructured":"Kari, Z. A. et al. Effect of fish meal substitution with fermented soy pulp on growth performance, digestive enzyme, amino acid profile, and immune-related gene expression of African catfish (Clarias gariepinus). Aquaculture 546, 737418. https:\/\/doi.org\/10.1016\/j.aquaculture.2021.737418 (2022).","journal-title":"Aquaculture"},{"key":"20433_CR74","doi-asserted-by":"publisher","first-page":"1548","DOI":"10.3390\/ijms18071548","volume":"18","author":"E M\u2019Kandawire","year":"2017","unstructured":"M\u2019Kandawire, E. et al. Metallothionein from wild populations of the African catfish Clarias gariepinus: from sequence, protein expression and metal binding properties to transcriptional biomarker of metal pollution. Int. J. Mol. Sci. 18, 1548. https:\/\/doi.org\/10.3390\/ijms18071548 (2017).","journal-title":"Int. J. Mol. Sci."},{"key":"20433_CR75","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1007\/s10499-021-00645-1","volume":"29","author":"H Nasrullah","year":"2021","unstructured":"Nasrullah, H. et al. Early immune gene development and expression in African catfish Clarias Gariepinus after challenged with Aeromonas hydrophila. Aquac Int. 29, 595\u2013607. https:\/\/doi.org\/10.1007\/s10499-021-00645-1 (2021).","journal-title":"Aquac Int."},{"key":"20433_CR76","doi-asserted-by":"publisher","first-page":"858","DOI":"10.1016\/j.fsi.2018.12.029","volume":"86","author":"Z Li","year":"2019","unstructured":"Li, Z., Wang, X., Chen, C., Gao, J. & Lv, A. Transcriptome profiles in the spleen of African catfish (Clarias gariepinus) challenged with Aeromonas veronii. Fish. Shellfish Immunol. 86, 858\u2013867. https:\/\/doi.org\/10.1016\/j.fsi.2018.12.029 (2019).","journal-title":"Fish. Shellfish Immunol."},{"key":"20433_CR77","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1111\/are.13552","volume":"49","author":"AM Samarin","year":"2018","unstructured":"Samarin, A. M. et al. mRNA abundance changes during in vitro oocyte ageing in African catfish Clarias Gariepinus (Burchell, 1822). Aquac Res. 49, 1037\u20131045. https:\/\/doi.org\/10.1111\/are.13552 (2018).","journal-title":"Aquac Res."},{"key":"20433_CR78","doi-asserted-by":"publisher","first-page":"739058","DOI":"10.1016\/j.aquaculture.2022.739058","volume":"564","author":"AN Abdel Rahman","year":"2023","unstructured":"Abdel Rahman, A. N. et al. Imidacloprid induced growth, hematological, neuro-behavior, anti-oxidant, economic, genetic, and histopathological alterations in Clarias gariepinus: alleviative role of dietary Hyphaene Thebaica. Aquaculture 564, 739058. https:\/\/doi.org\/10.1016\/j.aquaculture.2022.739058 (2023).","journal-title":"Aquaculture"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-20433-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-20433-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-20433-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T08:02:27Z","timestamp":1760256147000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-025-20433-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,7]]},"references-count":78,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["20433"],"URL":"https:\/\/doi.org\/10.1038\/s41598-025-20433-8","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,7]]},"assertion":[{"value":"5 June 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 September 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 October 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"35010"}}