PERTANIKA JOURNAL OF TROPICAL AGRICULTURAL SCIENCE

With a high likelihood of being discharged into aquatic habitats, zinc oxide nanoparticles have been widely employed in a variety of industrial and commercial goods. Concerns over their effects on the environment and human health have grown. This study evaluated the developmental toxicity of zinc oxide nanoparticles (ZnO NPs) on the embryo Java medaka (Oryzias javanicus). With three replicates for each treatment group, the Java medaka embryos were subject to various concentrations of ZnO NPs (10, 25, 50, 100, and 150 μg/L). The heartbeat of treated embryos was increased compared to the control group at 5-, 8-, and 11-days post-exposure (dpe). However, the hatching and mortality of embryos decreased when the concentrations of ZnO NPs increased. Meanwhile, deformities such as low pigmentation, edema (yolk sac and pericardial edema), and spinal deformities were observed in the embryo and larva during the exposure time. Compared to previous studies, ZnO NPs show severe toxicity to selected endpoints at lower concentrations in the embryos of Java medaka.

• Amal, M. N. A., Ismail, A., Saad, M. Z., Yasin, I. S. M., Nasruddin, N. S., Mastor, S. S., Rahman, M. H. A., & Mohamad, N. (2019). Study on Streptococcus agalactiae infection in Java medaka (Oryzias javanicus Bleeker, 1854) model. Microbial Pathogenesis, 131, 47-52. https://doi.org/10.1016/j.micpath.2019.03.034

• Amal, M. N. A., Zarif, S. T., Suhaiba, M. S., Aidil, M. R. M., Shaqinah, N. N., Zamri-Saad, M., & Ismail, A. (2018). The effects of fish gender on susceptibility to acute Streptococcus agalactiae infection in Java medaka Oryzias javanicus. Microbial Pathogenesis, 114, 251-254. https://doi.org/10.1016/j.micpath.2017.11.069

• Amin, N., Zulkifli, S. Z., Azmai, M. N. A., & Ismail, A. (2021). Toxicity of zinc oxide nanoparticles on the embryo of Java Medaka (Oryzias javanicus Bleeker, 1854): A comparative study. Animals, 11(8), 2170. https://doi.org/10.3390/ani11082170

• Asharani, P. V., Wu, Y. L., Gong, Z., & Valiyaveettil, S. (2008). Toxicity of silver nanoparticles in zebrafish models. Nanotechnology, 19(25), 255102. https://doi.org/10.1088/0957-4484/19/25/255102

• Ates, M., Daniels, J., Arslan, Z., Farah, I. O., & Rivera, H. F. (2013). Comparative evaluation of impact of Zn and ZnO nanoparticles on brine shrimp (Artemia salina) larvae: Effects of particle size and solubility on toxicity. Environmental Science: Processes and Impacts, 15(1), 225–233. https://doi.org/10.1039/C2EM30540B

• Aziz, S., Abdullah, S., Abbas, K., & Zia, M. A. (2020). Effects of engineered zinc oxide nanoparticles on freshwater fish, Labeo rohita: Characterization of ZnO nanoparticles, acute toxicity, and oxidative stress. Pakistan Veterinary Journal, 40(4), 479-483. https://doi.org/10.29261/pakvetj/2020.030

• Bai, W., Zhang, Z., Tian, W., He, X., Ma, Y., Zhao, Y., & Chai, Z. (2010). Toxicity of zinc oxide nanoparticles to zebrafish embryo: A physicochemical study of toxicity mechanism. Journal of Nanoparticle Research, 12, 1645-1654. https://doi.org/10.1007/s11051-009-9740-9

• Balbus, J. M., Maynard, A. D., Colvin, V. L., Castranova, V., Daston, G. P., Denison, R. A., Dreher, K. L., Goering, P. L., Goldberg, A. M., Kulinowski, K. M., Monteiro-Riviere, N. A., Oberdörster, G., Omenn, G. S., Pinkerton, K. E., Ramos, K. S., Rest, K. M., Sass, J. B., Silbergeld, E. K., & Wong, B. A. (2007). Meeting report: Hazard assessment for nanoparticles—Report from an interdisciplinary workshop. Environmental Health Perspectives, 115(11), 1654–1659. https://doi.org/10.1289/ehp.10327

• Blinova, I., Ivask, A., Heinlaan, M., Mortimer, M., & Kahru, A. (2010). Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environmental Pollution, 158(1), 41-47. https://doi.org/10.1016/j.envpol.2009.08.017

• Chen, P.-J., Wu, W.-L., & Wu, K. C.-W. (2013). The zerovalent iron nanoparticle causes higher developmental toxicity than its oxidation products in early life stages of medaka fish. Water Research, 47(12), 3899–3909. https://doi.org/10.1016/j.watres.2012.12.043

• Chen, T.-H., Lin, C.-C., & Meng, P.-J. (2014). Zinc oxide nanoparticles alter hatching and larval locomotor activity in zebrafish (Danio rerio). Journal of Hazardous Materials, 277, 134-140. https://doi.org/10.1016/j.jhazmat.2013.12.030

• Cong, Y., Jin, F., Wang, J., & Mu, J. (2017). The embryotoxicity of ZnO nanoparticles to marine medaka, Oryzias melastigma. Aquatic Toxicology, 185, 11–18. https://doi.org/10.1016/j.aquatox.2017.01.006

• Fernández, D., García-Gómez, C., & Babín, M. (2013). In vitro evaluation of cellular responses induced by ZnO nanoparticles, zinc ions and bulk ZnO in fish cells. Science of the Total Environment, 452–453, 262–274. https://doi.org/10.1016/j.scitotenv.2013.02.079

• García-Gómez, C., García-Gutiérrez, S., Obrador, A., & Fernández, M. D. (2020). Study of Zn availability, uptake, and effects on earthworms of zinc oxide nanoparticle versus bulk applied to two agricultural soils: Acidic and calcareous. Chemosphere, 239, 124814. https://doi.org/10.1016/j.chemosphere.2019.124814

• Gatti, A. M., Montanari, S., Monari, E., Gambarelli, A., Capitani, F., & Parisini, B. (2004). Detection of micro- and nano-sized biocompatible particles in the blood. Journal of Materials Science: Materials in Medicine, 15, 469–472. https://doi.org/10.1023/B:JMSM.0000021122.49966.6d

• Golling, G., Amsterdam, A., Sun, Z., Antonelli, M., Maldonado, E., Chen, W., Burgess, S., Haldi, M., Artzt, K., Farrington, S., Lin, S.-Y., Nissen, R. M., & Hopkins, N. (2002). Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nature Genetics, 31, 135–140. https://doi.org/10.1038/ng896

• Handy, R. D., von der Kammer, F., Lead, J. R., Hassellöv, M., Owen, R., & Crane, M. (2008). The ecotoxicology and chemistry of manufactured nanoparticles. Ecotoxicology, 17, 287-314. https://doi.org/10.1007/s10646-008-0199-8

• Hao, L., Chen, L., Hao, J., & Zhong, N. (2013). Bioaccumulation and sub-acute toxicity of zinc oxide nanoparticles in juvenile carp (Cyprinus carpio): A comparative study with its bulk counterparts. Ecotoxicology and Environmental Safety, 91, 52-60. https://doi.org/10.1016/j.ecoenv.2013.01.007

• Heinlaan, M., Ivask, A., Blinova, I., Dubourguier, H.-C., & Kahru, A. (2008). Toxicity of nanosized and bulk ZnO, CuO, and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere, 71(7), 1308-1316. https://doi.org/10.1016/j.chemosphere.2007.11.047

• Hou, J., Wu, Y., Li, X., Wei, B., Li, S., & Wang, X. (2018). Toxic effects of different types of zinc oxide nanoparticles on algae, plants, invertebrates, vertebrates, and microorganisms. Chemosphere, 193, 852–860. https://doi.org/10.1016/j.chemosphere.2017.11.077

• Imai, S., Koyama, J., & Fujii, K. (2007). Effects of estrone on full life cycle of Java medaka (Oryzias javanicus), a new marine test fish. Environmental Toxicology and Chemistry, 26(4), 726-731. https://doi.org/10.1897/05-539R2.1

• Ismail, A., & Yusof, S. (2011). Effect of mercury and cadmium on early life stages of Java medaka (Oryzias javanicus): A potential tropical test fish. Marine Pollution Bulletin, 63(5-12), 347-349. https://doi.org/10.1016/j.marpolbul.2011.02.014

• Iwamatsu, T., & Kobayashi, H. (2002). Electron microscopic observations of karyogamy in the fish egg. Development, Growth and Differentiation, 44(5), 357-363. https://doi.org/10.1046/j.1440-169X.2002.00649.x

• Kashiwada, S. (2006). Distribution of nanoparticles in the see-through medaka (Oryzias latipes). Environmental Health Perspectives, 114(11), 1697–1702. https://doi.org/10.1289/ehp.9209

• Kaya, H., Aydin, F., Gürkan, 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. https://doi.org/10.1016/j.chemosphere.2015.09.024

• Khandoga, A., Stampfl, A., Takenaka, S., Schulz, H., Radykewicz, R., Kreyling, W., & Krombach, F. (2004). Ultrafine particles exert prothrombotic but not inflammatory effects on the hepatic microcirculation in healthy mice in vivo. Circulation, 109(10), 1320–1325. https://doi.org/10.1161/01.CIR.0000118524.62298.E8

• Khoshnood, R., Jaafarzadeh, N., Jamili, S., Farshchi, P., & Taghavi, L. (2016). Acute toxicity of TiO2, CuO and ZnO nanoparticles in brine shrimp, Artemia franciscana. Iranian Journal of Fisheries Sciences, 16(4), 1287–1296.

• Kiener, T. K., Selptsova-Friedrich, I., & Hunziker, W. (2008). Tjp3/ZO-3 is critical for epidermal barrier function in zebrafish embryos. Developmental Biology, 316(1), 36–49. https://doi.org/10.1016/j.ydbio.2007.12.047

• Laban, G., Nies, L. F., Turco, R. F., Bickham, J. W., & Sepúlveda, M. S. (2010). The effects of silver nanoparticles on fathead minnow (Pimephales promelas) embryos. Ecotoxicology, 19, 185-195. https://doi.org/10.1007/s10646-009-0404-4

• Lee, K. J., Nallathamby, P. D., Browning, L. M., Osgood, C. J., & Xu, X.-H. N. (2007). In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano, 1(2), 133–143. https://doi.org/10.1021/nn700048y

• Li, J., Chen, Z., Huang, R., Miao, Z., Cai, L., & Du, Q. (2018). Toxicity assessment and histopathological analysis of nano-ZnO against marine fish (Mugilogobius chulae) embryos. Journal of Environmental Sciences, 73, 78-88. https://doi.org/10.1016/j.jes.2018.01.015

• Murthy, M, K., Mohanty, C, S., Swain, P., & Pattanayak, R. (2022). Assessment of toxicity in the freshwater tadpole Polypedates maculatus exposed to silver and zinc oxide nanoparticles: A multi-biomarker approach. Chemosphere, 293, 133511, https://doi.org/10.1016/j.chemosphere.2021.133511

• Organization for Economic Co-operation and Development. (2013). Test No. 210: Fish, early‐life stage toxicity test. OECD. https://www.oecd-ilibrary.org/docserver/9789264203785-en.pdf?expires=1715742309&id=id&accname=guest&checksum=DBDC65B79C5369E61BACCAD90C9B798C

• Patibandla, S., Zhang, Y., Tohari, A. M., Gu, P., Reilly, J., Chen, Y., & Shu, X. (2018). Comparative analysis of the toxicity of gold nanoparticles in zebrafish. Journal of Applied Toxicology, 38(8), 1153-1161. https://doi.org/10.1002/jat.3628

• Peters, A., Dockery, D. W., Muller, J. E., & Mittleman, M. A. (2001). Increased particulate air pollution and the triggering of myocardial infarction. Circulation, 103(23), 2810–2815. https://doi.org/10.1161/01.CIR.103.23.2810

• Peters, L. E., MacKinnon, M., Van Meer, T., van den Heuvel, M. R., & Dixon, D. G. (2007). Effects of oil sands process-affected waters and naphthenic acids on yellow perch (Perca flavescens) and Japanese medaka (Orizias latipes) embryonic development. Chemosphere, 67(11), 2177–2183. https://doi.org/10.1016/j.chemosphere.2006.12.034

• Rajkumar, K. S., Sivagaami, P., Ramkumar, A., Murugadas, A., Srinivasan, V., Arun, S., Kumar, P. S., & Thirumurugan, R. (2022). Bio-functionalized zinc oxide nanoparticles: Potential toxicity impact on freshwater fish Cyprinus carpio. Chemosphere, 290, 133220. https://doi.org/10.1016/j.chemosphere.2021.133220

• Rajput, V. D., Minkina, T. M., Behal, A., Sushkova, S. N., Mandzhieva, S., Singh, R., Gorovtsov, A., Tsitsuashvili, V. S., Purvis, W. O., Ghazaryan, K. A., & Movsesyan, H. S. (2018). Effects of zinc-oxide nanoparticles on soil, plants, animals, and soil organisms: A review. Environmental Nanotechnology, Monitoring and Management, 9, 76-84. https://doi.org/10.1016/j.enmm.2017.12.006

• Sabir, S., Arshad, M., & Chaudhari, S. K. (2014). Zinc oxide nanoparticles for revolutionizing agriculture: Synthesis and applications. The Scientific World Journal, 2014, 925494. https://doi.org/10.1155/2014/925494

• Salleh, A. F. M., Amal, M. N. A., Nasruddin, N. S., Zulkifli, S. Z., Yusuff, F. M., Ibrahim, W. N. W., & Ismail, A. (2017). Water pH effects on survival, reproductive performances, and ultrastructure of gonads, gills, and skins of the Java medaka (Oryzias javanicus). Turkish Journal of Veterinary and Animal Sciences, 41(4), 471-481. https://doi.org/10.3906/vet-1701-9

• Sirelkhatim, A., Mahmud, S., Seeni, A., Kaus, N. H. M., Ann, L. C., Bakhori, S. K. M., Hasan, H., & Mohamad, D. (2015). Review on zinc oxide nanoparticles: Antibacterial activity and toxicity mechanism. Nano-Micro Letters, 7, 219–242. https://doi.org/10.1007/s40820-015-0040-x

• Suman, T. Y., Radhika Rajasree, S. R., & Kirubagaran, R. (2015). Evaluation of zinc oxide nanoparticles toxicity on marine algae Chlorella vulgaris through flow cytometric, cytotoxicity and oxidative stress analysis. Ecotoxicology and Environmental Safety, 113, 23–30. https://doi.org/10.1016/j.ecoenv.2014.11.015

• Taherian, S. M. R., Hosseini, S. A., Jafari, A., Etminan, A., & Birjandi, M. (2019). Acute toxicity of zinc oxide nanoparticles from Satureja hortensis on rainbow trout (Oncorhynchus mykiss). Turkish Journal of Fisheries and Aquatic Sciences, 20(6), 481-489. https://doi.org/10.4194/1303-2712-v20_6_06

• Wittbrodt, J., Shima, A., & Schartl, M. (2002). Medaka - A model organism from the far east. Nature Reviews Genetics, 3, 53-64. https://doi.org/10.1038/nrg704

• Wong, S. W. Y., Leung, P. T. Y, Djurišić, A. B., & Leung, K. M. Y. (2010). Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Analytical and Bioanalytical Chemistry, 396, 609-618. https://doi.org/10.1007/s00216-009-3249-z

• Woo, S., & Yum, S. (2011). Transcriptional response of marine medaka (Oryzias javanicus) on exposure to toxaphene. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 153(3), 355-361. https://doi.org/10.1016/j.cbpc.2010.12.006

• Wu, Y., & Zhou, Q. (2012). Dose- and time-related changes in aerobic metabolism, chorionic disruption, and oxidative stress in embryonic medaka (Oryzias latipes): Underlying mechanisms for silver nanoparticle developmental toxicity. Aquatic Toxicology, 124–125, 238–246. https://doi.org/10.1016/j.aquatox.2012.08.009

• Wu, Y., Zhou, Q., Li, H., Liu, W., Wang, T., & Jiang, G. (2010). Effects of silver nanoparticles on the development and histopathology biomarkers of Japanese medaka (Oryzias latipes) using the partial-life test. Aquatic Toxicology, 100(2), 160-167. https://doi.org/10.1016/j.aquatox.2009.11.014

• Xiao, Y., Vijver, M. G., Chen, G., & Peijnenburg, W. J. G. M. (2015). Toxicity and accumulation of Cu and ZnO nanoparticles in Daphnia magna. Environmental Science and Technology, 49(7), 4657–4664. https://doi.org/10.1021/acs.est.5b00538

• Xiong, D., Fang, T., Yu, L., Sima, X., & Zhu, W. (2011). Effects of nano-scale TiO2, ZnO, and their bulk counterparts on zebrafish: Acute toxicity, oxidative stress and oxidative damage. Science of the Total Environment, 409(8), 1444-1452. https://doi.org/10.1016/j.scitotenv.2011.01.015

• Yu, J.-F., Fukamachi, S., Mitani, H., Hori, H., & Kanamori, A. (2006). Reduced expression of vps11 causes less pigmentation in medaka, Oryzias latipes. Pigment Cell Research, 19(6), 628–634. https://doi.org/10.1111/j.1600-0749.2006.00346.x

• Zhao, X., Wang, S., Wu, Y., You, H., & Lv, L. (2013). Acute ZnO nanoparticles exposure induces developmental toxicity, oxidative stress, and DNA damage in embryo-larval zebrafish. Aquatic Toxicology, 136-137, 49-59. https://doi.org/10.1016/j.aquatox.2013.03.019

• Zhu, X., Wang, J., Zhang, X., Chang, Y., & Chen, Y. (2009). The impact of ZnO nanoparticle aggregates on the embryonic development of zebrafish (Danio rerio). Nanotechnology, 20(19), 195103. https://doi.org/10.1088/0957-4484/20/19/195103

• Zhu, X., Zhu, L., Duan, Z., Qi, R., Li, Y., & Lang, Y. (2008). Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to zebrafish (Danio rerio) early developmental stage. Journal of Environmental Science and Health, Part A, 43(3), 278-284. https://doi.org/10.1080/10934520701792779