Assessing the Toxicity of Benzalkonium Chloride on Common Carp (Cyprinus carpio): Impacts on Blood Cells, Gills, Intestines, and Liver

Document Type : Original Research Article

Authors

Department of Environmental Engineering, Faculty of Natural Resources and Environment, University of Birjand, Birjand, Iran

Abstract

The use of Benzalkonium Chloride and other alternative disinfectants increased during the COVID-19 pandemic. Therefore, it is crucial to consider their environmental effects. This study aims to investigate the toxicity potential of different concentrations of Benzalkonium Chloride on the blood cells, gills, intestines, and liver of common carp. For this purpose, 50 fish were divided into 5 groups of 10 (including one control group) and exposed to BAC concentrations of 0.10, 0.32, 0.58, and 0.75 mg/L for 28 days. The results showed that the RBC count (millions/mm³) in all exposed groups (Group B: 9.6 ± 1.07; Group C: 8.7 ± 0.78; Group D: 7.4 ± 0.96; Group E: 6.9 ± 0.55) was significantly lower (p<0.05) than in the control group (13.9 ± 1.25). The cholesterol, triglyceride, protein, and albumin levels (mg/dl) in all experimental groups were lower than those in the control group. Conversely, the AST levels in all exposed groups were significantly higher (P<0.05) compared to the control group. Gill damage included lamellar fusion, curvature, edema, and necrosis. In the liver, histological damage consisted of hepatocyte degeneration, central vein wall rupture, melano-macrophage aggregation, and blood vessel dilation. The results indicate that as Benzalkonium Chloride concentration increases from 0.10 to 0.78 mg/L, its toxicity effects on common carp also intensify. Therefore, before incorporating Benzalkonium Chloride into commercial products like cosmetics, its toxic effects should be thoroughly assessed to mitigate environmental harm.

Keywords

Main Subjects

References

Alkaladi, A., El-Deen, N. A. N., Afifi, M. & Zinadah, O.A.A., 2015. Hematological and biochemical investigations on the effect of vitamin E and C on Oreochromis niloticus exposed to zinc oxide nanoparticles. Saudi Journal of Biological Sciences, 22(5), 556-563.
Abd El-Naby, A.S., Al-Sagheer, A.A., Negm, S.S. & Naiel, M.A., 2020. Dietary combination of chitosan nanoparticle and thymol affects feed utilization, digestive enzymes, antioxidant status, and intestinal morphology of Oreochromis niloticus. Aquaculture, 515, 734577.
Arman, S., 2021. Effects of acute triclosan exposure on gill and liver tissues of zebrafish (Danio rerio). In Annales de Limnologie-international journal of limnology (Vol. 57, p. 6). EDP Sciences.
adel Abdel-Khalek, A., Kadry, M., Hamed, A. & Marie, M.A., 2015. Ecotoxicological impacts of zinc metal in comparison to its nanoparticles in Nile tilapia; Oreochromis niloticus. The Journal of Basic & Applied Zoology, 72, 113-125.
Akram, R., Ghaffar, A., Hussain, R., Khan, I., de Assis Santana, V.L., Mehmood, K. ... & Zhu, H., 2022. Hematological, serum biochemistry, histopathological and mutagenic impacts of triclosan on fish (bighead carp). Agrobiological Records, 7, 18-28.
Akram, R., Iqbal, R., Hussain, R., Jabeen, F. & Ali, M., 2021. Evaluation of oxidative stress, antioxidant enzymes and genotoxic potential of bisphenol A in fresh water bighead carp (Aristichthys nobils) fish at low concentrations. Environmental Pollution, 268, 115896.
Antunes, S.C., Nunes, B., Rodrigues, S., Nunes, R., Fernandes, J. & Correia, A.T., 2016. Effects of chronic exposure to benzalkonium chloride in Oncorhynchus mykiss: cholinergic neurotoxicity, oxidative stress, peroxidative damage and genotoxicity. Environmental Toxicology and Pharmacology, 45, 115-122.
Artacho, P., Soto-Gamboa, M., Verdugo, C. & Nespolo, R.F., 2007. Blood biochemistry reveals malnutrition in black-necked swans (Cygnus melanocoryphus) living in a conservation priority area. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 146(2), 283-290.
Aboulhoda, B.E., Abdeltawab, D.A., Rashed, L.A., Abd Alla, M.F. & Yassa, H.D., 2020. Hepatotoxic Effect of Oral Zinc Oxide Nanoparticles and the Ameliorating Role of Selenium in Rats: A histological, immunohistochemical and molecular study. Tissue and Cell, 67, 101441.
Antunes, S.C., Nunes, B., Rodrigues, S., Nunes, R., Fernandes, J. & Correia, A.T., 2016. Effects of chronic exposure to benzalkonium chloride in Oncorhynchus mykiss: cholinergic neurotoxicity, oxidative stress, peroxidative damage and genotoxicity. Environmental Toxicology and Pharmacology, 45, 115-122.
Arianto, S.R., Syah, F.A., Sari, L.A., Nafisyah, A.L., Arsad, S. & Musa, N., 2023. Analyze the toxicities of benzalkonium chloride as a COVID-19 disinfectant in physiological goldfish (Carassius auratus). Veterinary World, 16(7), 1400.
Bera, K.K., Kumar, S., Paul, T., Prasad, K.P., Shukla, S.P. & Kumar, K., 2020. Triclosan induces immunosuppression and reduces survivability of striped catfish Pangasianodon hypophthalmus during the challenge to a fish pathogenic bacterium Edwardsiella tarda. Environmental Research, 186, 109575.
Bongers, A.B.J., Sukkel, M., Gort, G., Komen, J. & Richter, C.J.J., 1998. Development and use of genetically uniform strains of common carp in experimental animal research. Laboratory Animals, 32(4), 349-363.
Choi, H.Y., Lee, Y.H., Lim, C.H., Kim, Y.S., Lee, I.S., Jo, J.M. ... & Seo, D.S., 2020. Assessment of respiratory and systemic toxicity of Benzalkonium chloride following a 14-day inhalation study in rats. Particle and Fibre Toxicology, 17, 1-19.
Christen, V., Faltermann, S., Brun, N.R., Kunz, P.Y. & Fent, K., 2017. Cytotoxicity and molecular effects of biocidal disinfectants (quaternary ammonia, glutaraldehyde, poly (hexamethylene biguanide)
hydrochloride PHMB) and their mixtures in vitro and in zebrafish eleuthero-embryos. Science of the Total Environment, 586, 1204-1218.
Chupani, L., Zuskova, E., Niksirat, H., Panacek, A., Lünsmann, V., Haange, S.B. ... & Jehmlich, N., 2017. Effects of chronic dietary exposure of zinc oxide nanoparticles on the serum protein profile of juvenile common carp (Cyprinus carpio L.). Science of The Total Environment, 579, 1504-1511.
Curi, L.M., Peltzer, P.M., Sandoval, M.T. & Lajmanovich, R.C., 2019. Acute toxicity and sublethal effects caused by a commercial herbicide formulated with 2, 4-D on Physalaemus albonotatus tadpoles. Water, Air, & Soil Pollution, 230, 1-15.
de Souza, T.A.J., Souza, L.R.R. & Franchi, L.P., 2019. Silver nanoparticles: An integrated view of green synthesis methods, transformation in the environment, and toxicity. Ecotoxicology and Environmental Safety, 171, 691-700.
Capkin, E., Ozcelep, T., Kayis, S. & Altinok, I., 2017. Antimicrobial agents, triclosan, chloroxylenol, methylisothiazolinone and borax, used in cleaning had genotoxic and histopathologic effects on rainbow trout. Chemosphere, 182, 720-729.
Chai, L., Chen, A., Luo, P., Zhao, H. & Wang, H., 2017. Histopathological changes and lipid metabolism in the liver of Bufo gargarizans tadpoles exposed to Triclosan. Chemosphere, 182, 255-266.
Clara, M., Scharf, S., Scheffknecht, C. & Gans, O., 2007. Occurrence of selected surfactants in untreated and treated sewage. Water Research, 41(19), 4339-4348.
Dar, O.I., Vinothkanna, A., Aslam, B., Furkh, A., Sharma, S., Kaur, A. ... & Jia, A.Q., 2024. Dynamic alterations in physiological and biochemical indicators of Cirrhinus mrigala hatchlings: A sublethal exposure of triclosan. Science of The Total Environment, 924, 171701.
Dani, U., Bahadur, A. & Kuperkar, K., 2019. Biotoxicity and tissue-specific oxidative stress induced by Gemini surfactant as a protocol on fingerlings of Cirrhinus mrigala (Ham.): An integrated experimental and theoretical methodology. Ecotoxicology and Environmental Safety, 183, 109478.
Dar, O.I., Sharma, S., Singh, K., Sharma, A., Bhardwaj, R. & Kaur, A., 2020a. Biomarkers for the toxicity of sublethal concentrations of triclosan to the early life stages of carps. Scientific Reports, 10(1), 17322.
Dar, O. I., Sharma, S., Singh, K., Sharma, A., Bhardwaj, R. & Kaur, A., 2020b. Biochemical markers for prolongation of the acute stress of triclosan in the early life stages of four food fishes. Chemosphere, 247, 125914.
Das, A. & Mohanty, P.K., 2018. Comparative hemocytobiochemical profile of Rattus rattus Linnaeus, 1758 and Rattus norvegicus Berkenhout, 1769. Comparative Clinical Pathology, 27, 1509-1514.
Elkeiy, M.M., Khamis, A.A., El-Gamal, M.M., Abo Gazia, M.M., Zalat, Z.A. & El-Magd, M.A., 2020. Chitosan nanoparticles from Artemia salina inhibit progression of hepatocellular carcinoma in vitro and in vivo. Environmental Science and Pollution Research, 27, 19016-19028.
Food and Drug Adminnistration, H.H.S., 2016. Safety and effectiveness of consumer antiseptics; topical antimicrobial drug products for over-the-counter human use. Final rule. Federal Register, 81(172), 61106-61130.
Ferk, F., Misik, M., Hoelzl, C., Uhl, M., Fuerhacker, M., Grillitsch, B. ... & Knasmüller, S., 2007. Benzalkonium chloride (BAC) and dimethyldioctadecyl-ammonium bromide (DDAB), two common quaternary ammonium compounds, cause genotoxic effects in mammalian and plant cells at environmentally relevant concentrations. Mutagenesis, 22(6), 363-370.
Gouda, A.M., Hagras, A.E., Okbah, M.A. & El-Gammal, M.I., 2022. Influence of the Linear Alkylbenzene Sulfonate (LAS) on hematological and biochemical parameters of Nile Tilapia, Oreochromis niloticus. Saudi Journal of Biological Sciences, 29(2), 1006-1013.
Giang, P.T., Burkina, V., Sakalli, S., Schmidt-Posthaus, H., Rasmussen, M.K., Randak, T. ... & Zlabek, V., 2019. Effects of multi-component mixtures from sewage treatment plant effluent on common carp (Cyprinus carpio) under fully realistic condition. Environmental Management, 63, 466-484.
Ghaffar, A., Hussain, R., Abbas, G., Kalim, M., Khan, A., Ferrando, S. ... & Ahmed, Z., 2018. Fipronil (Phenylpyrazole) induces hemato-biochemical, histological and genetic damage at low doses in common carp, Cyprinus carpio (Linnaeus, 1758). Ecotoxicology, 27, 1261-1271.
Ghaffar, A., Hussain, R., Ahmad, N., Ghafoor, R., Akram, M.W., Khan, I. & Khan, A., 2021. Evaluation of hemato-biochemical, antioxidant enzymes as biochemical biomarkers and genotoxic potential of glyphosate in freshwater fish (Labeo rohita). Chemistry and Ecology, 37(7), 646-667.
Gheorghe, S., Mitroi, D.N., Stan, M.S., Staicu, C.A., Cicirma, M., Lucaciu, I.E. ... & Dinischiotu, A., 2020. Evaluation of sub-lethal toxicity of benzethonium chloride in Cyprinus carpio liver. Applied Sciences, 10(23), 8485.
Hedayati, S.A., Farsani, H.G., Naserabad, S.S., Hoseinifar, S.H. & Van Doan, H., 2019. Protective effect of dietary vitamin E on immunological and biochemical induction through silver nanoparticles (AgNPs) inclusion in diet and silver salt (AgNO3) exposure on Zebrafish (Danio rerio). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 222, 100-107.
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.
Hatami, M., Banaee, M. & Haghi, B.N., 2019. Sub-lethal toxicity of chlorpyrifos alone and in combination with polyethylene glycol to common carp (Cyprinus carpio). Chemosphere, 219, 981-988.
Hemalatha, D., Rangasamy, B., Nataraj, B. & Ramesh, M., 2019. Assessment of triclosan impact on enzymatic biomarkers in an Indian major carp, Catla catla. The Journal of Basic and Applied Zoology, 80, 1-8.
Ikisa, K.G., Babatunde, B.B. & Hart, A.I., 2019. Histopathological variations in gills, liver and kidney of Nile tilapia-Oreochromis niloticus exposed to benzalkoniumbhloride mixture with treated produced water. Journal of Applied Sciences and Environmental Management, 23(6), 1181-1187.
Julinta, R.B., Abraham, T.J., Roy, A., Singha, J., Boda, S. & Patil, P.K., 2019. Dietary influences of oxytetracycline on the growth and serum biomarkers of Oreochromis niloticus (L.). Ecotoxicology and Environmental Safety, 186, 109752.
Johari, S.A., Kalbassi, M.R., Yu, I.J. & Lee, J.H., 2015. Chronic effect of waterborne silver nanoparticles on rainbow trout (Oncorhynchus mykiss): histopathology and bioaccumulation. Comparative Clinical Pathology, 24, 995-1007.
Jee, J.H. & Kang, J.C., 2005. Biochemical changes of enzymatic defense system after phenanthrene exposure in olive flounder, Paralichthys olivaceus. Physiological Research, 54(585), e591.
Kaya, H., Celik, E.S., Yılmaz, S., Tulgar, A., Akbulut, M. & Demir, N., 2015. Hematological, serum biochemical, and immunological responses in common carp (Cyprinus carpio) exposed to phosalone. Comparative Clinical Pathology, 24, 497-507.
Kaya, H., Aydın, F., Gurkan, M., Yılmaz, S., Ates, M., Demir, V. & Arslan, Z., 2016. A comparative toxicity study between small and large size zinc oxide nanoparticles in tilapia (Oreochromis niloticus): Organ pathologies, osmoregulatory responses and immunological parameters. Chemosphere, 144, 571-582.
Kakakhel, M.A., Wu, F., Sajjad, W., Zhang, Q., Khan, I., Ullah, K. & Wang, W., 2021. Long-term exposure to high-concentration silver nanoparticles induced toxicity, fatality, bioaccumulation, and histological alteration in fish (Cyprinus carpio). Environmental Sciences Europe, 33, 1-11.
Kaczerewska, O., Martins, R., Figueiredo, J., Loureiro, S. & Tedim, J., 2020. Environmental behaviour and ecotoxicity of cationic surfactants towards marine organisms. Journal of Hazardous Materials, 392, 122299.
Kwon, D., Kwon, J.T., Lim, Y.M., Shim, I., Kim, E., Lee, D.H. ... & Kim, H.M., 2019. Inhalation toxicity of benzalkonium chloride and triethylene glycol mixture in rats. Toxicology and Applied Pharmacology, 378, 114609.
Kwon, Y.S., Jung, J. W., Kim, Y.J., Park, C.B., Shon, J.C., Kim, J.H. ... & Seo, J.S., 2020. Proteomic analysis of whole-body responses in medaka (Oryzias latipes) exposed to benzalkonium chloride. Journal of Environmental Science and Health, Part A, 55(12), 1387-1397.
Kandel, I. & Castelli, M., 2020. A novel architecture to classify histopathology images using convolutional neural networks. Applied Sciences, 10(8), 2929.
Lavorgna, M., Russo, C., D'Abrosca, B., Parrella, A. & Isidori, M., 2016. Toxicity and genotoxicity of the quaternary ammonium compound benzalkonium chloride (BAC) using Daphnia magna and Ceriodaphnia dubia as model systems. Environmental Pollution, 210, 34-39.
Li, M.H., 2008. Effects of nonionic and ionic surfactants on survival, oxidative stress, and cholinesterase activity of planarian. Chemosphere, 70(10), 1796-1803.
Lakra, K.C., Banerjee, T.K. & Lal, B., 2021. Coal mine effluent-induced metal bioaccumulation, biochemical, oxidative stress, metallothionein, and histopathological alterations in vital tissues of the catfish, Clarias batrachus. Environmental Science and Pollution Research, 28, 25300-25315.
Li, W., Zhang, W., Chang, M., Ren, J., Xie, W., Chen, H. ... & Li, H., 2018. Metabonomics reveals that triclocarban affects liver metabolism by affecting glucose metabolism, β-oxidation of fatty acids, and the TCA cycle in male mice. Toxicology Letters, 299, 76-85.
Merchel Piovesan Pereira, B. & Tagkopoulos, I., 2019. Benzalkonium chlorides: uses, regulatory status, and microbial resistance. Applied and Environmental Microbiology, 85(13), e00377-19.
Mentese, E., & Hancer, E., 2020. Histopatoloji görüntülerde derin öğrenme yöntemleri ile çekirdek segmentasyonu. Avrupa Bilim ve Teknoloji Dergisi, 95-102.
Martinez-Carballo, E., Sitka, A., Gonzalez-Barreiro, C., Kreuzinger, N., Furhacker, M., Scharf, S. & Gans, O., 2007. Determination of selected quaternary ammonium compounds by liquid chromatography with mass spectrometry. Part I. Application to surface, waste and indirect discharge water samples in Austria. Environmental Pollution, 145(2), 489-496.
Mansouri, B., Maleki, A., Johari, S.A., Shahmoradi, B., Mohammadi, E. & Davari, B., 2017. Histopathological effects of copper oxide nanoparticles on the gill and intestine of common carp (Cyprinus carpio) in the presence of titanium dioxide nanoparticles. Chemistry and Ecology, 33(4), 295-308.
Nan, Y., Zhu, X., Huang, J., Zhang, Z., Xing, Y., Yang, Y. ... & Duan, Y., 2023. Toxic effects of triclocarban on the histological morphology, physiological and immune response in the gills of the black tiger shrimp Penaeus monodon. Marine Environmental Research, 192, 106245.
Owonikoko, M.W., Salami, A.T., Odukanmi, A.O., Emikpe, B.O. & Olaleye, S.B., 2022. Hematopoietic toxicity in wistar rats experimentally exposed to cement dust. Comparative Clinical Pathology, 31(2), 181-199.
O'Brown, N.M., Pfau, S.J. & Gu, C., 2018. Bridging barriers: a comparative look at the blood–brain barrier across organisms. Genes & Development, 32(7-8), 466-478.
OECD., 2019. OECD Guidelines for the Testing of Chemicals, Section 2: Effects on Biotic Systems, Test guideline No. 203: Fish, Acute Toxicity Testing. OECD Publishing, https://doi.org/10.1787/20745761.
Pourahmad, J., Salami, M. & Zarei, M.H., 2023. Comparative toxic effect of bulk copper oxide (CuO) and CuO nanoparticles on human red blood cells. Biological Trace Element Research, 201(1), 149-155.
Perez, P., Fernandez, E. & Beiras, R., 2009. Toxicity of benzalkonium chloride on monoalgal cultures and natural assemblages of marine phytoplankton. Water, Air, and Soil Pollution, 201, 319-330.
Penuela, G. A., & Martinez-Lopez, E., 2021. Enzymatic activity changes in striped catfish Pseudoplatystoma magdaleniatum, induced by exposure to different concentrations of ibuprofen and triclosan. Chemosphere, 271, 129399.
Pane, E.F., Haque, A. & Wood, C.M., 2004. Mechanistic analysis of acute, Ni-induced respiratory toxicity in the rainbow trout (Oncorhynchus mykiss): an exclusively branchial phenomenon. Aquatic Toxicology, 69(1), 11-24.
Priyatha, C.V. & Chitra, K.C., 2018. Acute toxicity of triclosan on the native freshwater fish, Anabas testudineus (Bloch, 1792): behavioral alterations and histopathological lesions. International Journal of Life Sciences, 6(1), 166-172.
Rodrigues, S., Antunes, S.C., Nunes, B. & Correia, A.T., 2019. Histopathological effects of the antibiotic erythromycin on the freshwater fish species Oncorhynchus mykiss. Ecotoxicology and Environmental Safety, 181, 1-10.
Sharma, S., Dar, O.I., Singh, K., Kaur, A. & Faggio, C., 2021. Triclosan elicited biochemical and transcriptomic alterations in Labeo rohita larvae. Environmental Toxicology and Pharmacology, 88, 103748.
Said, R.E., Abd–ElRaouf, M.H., Moustafa, M.A. & Badrey, A.E., 2023. Hemato-Serological Findings as Early signals in Nile Tilapia Oreochromis niloticus Treated with Benzalkonium Chloride. Baghdad Science Journal, 20(3 (Suppl.)), 0945-0945.
Shaluei, F., Hedayati, A., Jahanbakhshi, A., Kolangi, H. & Fotovat, M., 2013. Effect of subacute exposure to silver nanoparticle on some hematological and plasma biochemical indices in silver carp (Hypophthalmichthys molitrix). Human & Experimental Toxicology, 32(12), 1270-1277.
Suganthi, P., Murali, M., Sadiq Bukhari, A., Syed Mohamed, H.E., Basu, H. & Singhal, R.K., 2015. Behavioural and Histological variations in Oreochromis mossambicus after exposure to ZnO Nanoparticles. International Journal of Applied Research, 1(8), 524-31.
Saravanan, M., Karthika, S., Malarvizhi, A. & Ramesh, M., 2011. Ecotoxicological impacts of clofibric acid and diclofenac in common carp (Cyprinus carpio) fingerlings: hematological, biochemical, ionoregulatory and enzymological responses. Journal of Hazardous Materials, 195, 188-194.
Tuncsoy, M., 2021. Impacts of titanium dioxide nanoparticles on serum parameters and enzyme activities of Clarias gariepinus. Bulletin of Environmental Contamination and Toxicology, 106(4), 629-636.
Vasantharaja, D., Ramalingam, V. & Reddy, G.A., 2015. Oral toxic exposure of titanium dioxide nanoparticles on serum biochemical changes in adult male Wistar rats. Nanomedicine Journal, 2(1).
Vijitha, C.K., Asifa, K.P. & Chitra, K.C., 2017. Assessment of genotoxic and haematological consequence of triclosan in the fish, Oreochromis niloticus (Linnaeus, 1758). International Journal of Applied Research, 3(2), 101-109.
Yahya, R.A., Attia, A.M., El-Banna, S.G., El-Trass, E.E., Azab, A.E., Jbireal, J.M. & Shkal, K.E.M., 2019. Hematotoxicity induced by copper oxide and/or zinc oxide nanoparticles in male albino rats. Journal Biotechnol, 3(4), 1-7.
Zheng, H., Mortensen, L.J. & DeLouise, L.A., 2013. Thiol antioxidant-functionalized CdSe/ZnS quantum dots: synthesis, characterization, cytotoxicity. Journal of Biomedical Nanotechnology, 9(3), 382-392.
Zheng, G., Filippelli, G.M. & Salamova, A., 2020. Increased indoor exposure to commonly used disinfectants during the COVID-19 pandemic. Environmental Science & Technology Letters, 7(10), 760-765.
Zhang, C., Cui, F., Zeng, G.M., Jiang, M., Yang, Z.Z., Yu, Z.G. ... & Shen, L.Q., 2015. Quaternary ammonium compounds (QACs): A review on occurrence, fate and toxicity in the environment. Science of the Total Environment, 518, 352-362.
Zhang, L., Yang, Z., Yang, M., Yang, F., Wang, G., Liu, D. ... & Wang, Z., 2022. Copper-induced oxidative stress, transcriptome changes, intestinal microbiota, and histopathology of common carp (Cyprinus carpio). Ecotoxicology and Environmental Safety, 246, 114136.
Zhang, C., Cui, F., Zeng, G.M., Jiang, M., Yang, Z.Z., Yu, Z.G. ... & Shen, L.Q., 2015. Quaternary ammonium compounds (QACs): A review on occurrence, fate and toxicity in the environment. Science of the Total Environment, 518, 352-362.           

Files

Share

How to cite

Statistics