Effect of feeding honey bees Apis mellifera with nanocerium dioxide on the mineral composition of honey, wax and the bees’ bodies

  • L. M. Nikitina National Scientific Center
  • D. A. Zasekin National University of Life and Environmental Sciences of Ukraine
  • L. V. Shevchenko National University of Life and Environmental Sciences of Ukraine
  • N. M. Zholobak Zabolotny Institute of Microbiology and Virology
  • V. O. Postoenko National Scientific Center
  • I. M. Andrusyshyna Kundiiev Institute of Occupational Health of the NAMS
  • N. Morfin University of Manitoba
  • N. H. Grushanska National University of Life and Environmental Sciences of Ukraine
  • T. M. Yefimenko Zabolotny Institute of Microbiology and Virology
  • H. V. Odnosum Zabolotny Institute of Microbiology and Virology
  • H. V. Postoenko National Scientific Center
Keywords: beekeeping products, microelements, macroelements, nanoproducts, cerium, magnesium, zinc, selenium.

Abstract

Restrictions or complete prohibition of antibiotic use in livestock production, and particularly in beekeeping, r e quire the search for alternative means to control infectious diseases in honey bee colonies. Therefore, nanotechnology products are gaining importance as they are capable of enhancing bees’ resistance to diseases by disrupting bacterial cell walls or membranes at low concentrations, while potentially remaining safe for humans and the environment. Nanocerium dioxide (nano-CeO 2 ) is one such nanoproduct with these properties, including acting as antioxidant and antibacterial agent. Although nano-CeO 2 has been identified as a potential product against infectious diseases in honey bees, there is no information on its effects on honey composition and hive products, nor its broader impact on honey bee health. Thus, the aim of the study was to evaluate the quality of honey and the mineral composition of bee bodies, honey, and wax following the feeding of bee colonies with nano-CeO2 via sugar syrup. For the experiment, control and experimental groups of medium-strength bee colonies were formed at the NSC Institute of B eekeeping named after P. I. Prokopovich (Kyiv, Ukraine). Colonies in the experimental group were fed sugar syrup supplemented with nano-CeO 2 at a concentration of 1 mM, while the control group received syrup without the nano-additive. The exp e riment assessed honey quality indicators, such as diastase activity, as well as the content of Ce, Mg, Zn, and Se in bees’ bodies, honey, and wax using inductively coupled plasma optical emission spectroscopy. Feeding bee colonies with sugar syrup containing nano-CeO 2 did not affect the levels of water, proline, Mg, or Zn in honey but increased its diastase activity by 32.8%. Feeding bees nano-CeO 2 increased Ce content by 2.84-fold and decreased Se content by 24.1% in bee bodies, forming the following order of mineral component distribution: Mg > Zn > Ce > Se. The use of nano-CeO 2 in bee colonies did not affect the accumulation of Mg, Zn, or Se in honey, but increased the Ce content by 19.14-fold. Under the influence of nano-CeO2, Ce content increased 1.51-fold and Se content 1.91-fold in wax. Ce concentration in honey showed a strong positive correlation with its content in bee bodies, whereas Se content in bee bodies showed a strong inverse correlation with its level in wax. Spring feeding of bee colonies with sugar syrup supplemented with nano-CeO 2 showed no effect on the main honey quality indicators, while demonstrating a high capacity for Ce accumulation in bees’ bodies, honey, and wax. Overall, these findings provide a foundation for the development of functional and safe treatment products against bee diseases, as well as beekeeping products enriched with nano-CeO 2 as an antimicrobial agent.

References

Abou-Shaara, H, F., Staron, M., & Staroňová, D. (2020). Potential applications of nanotechnology in apiculture. Entomology and Applied Science Letters, 7(4), 1–8.

Abou-Shaara, H. F., Staron, M., & Staroňová, D. (2021). Exploring the role of nanotechnology in enhancing apiculture practices. International Journal of Veterinary Research and Allied Sciences, 1(1), 1–8.

Aljedani, D. M. (2020). Revealing some elements and heavy metals in honeybee and beeswax samples collected from different environments. Entomology and Applied Science Letters, 7(4), 89–101.

Arslan, K., & Akbaba, G. B. (2020). In vitro genotoxicity assessment and comparison of cerium (IV) oxide micro- and nanoparticles. Toxicology and Industrial Health, 36(2), 76–83.

Balasooriya, E. R., Jayasinghe, C. D., Jayawardena, U. A., Ruwanthika, R. W. D., Mendis de Silva, R., & Udagama, P. V. (2017). Honey mediated green synthesis of nanoparticles: New era of safe nanotechnology. Journal of Nanomaterials, 2017(1), 5919836.

Bayer, O. V., Yaremchuk, O. S., Yevtushenko, T. V., Shevchenko, L. V., Mykhalska, V. M., Dobrozhan, Y. V., Dovhopol, Y., V., & Varpikhovskyi, R. L. (2018). Rozrobka ta otsinka prydatnosti metodu vyznachennia nitrofuraniv v medi za dopomohoiu ridynnoyi khromatohrafiyi vysokoho tysku – tandemnoyi mas-spektrometriyi (UPLC-RS-RS) [The development and validation of a rapid method for the determination of nitrofurans in honey using high pressure liquid chromatography tandem mass spectrometry (UPLC MS MS)]. Ukrainian Journal of Ecology, 8(1), 966–974 (in Ukrainian).

Bouhlali, E. D. T., Bammou, M., Sellam, K., El Midaoui, A., Bourkhis, B., Ennassir, J., El Midaoui, A., Filali-Zegzouti, Y. (2019). Physicochemical properties of eleven monofloral honey samples produced in Morocco. Arab Journal of Basic and Applied Sciences, 26(1), 476–487.

Charbgoo, F., Ahmad, M. B., & Darroudi, M. (2017). Cerium oxide nanoparticles: Green synthesis and biological applications. International Journal of Nanomedicine, 12, 1401–1413.

Constantin, M., Chioncel, M., Petrescu, L., Vrancianu, C., Paun, M., Cristian, R., Sidoroff, M., Dionisie, M., & Chifiriuc, M. (2025). From rock to living systems: Lanthanides toxicity and biological interactions. Ecotoxicology and Environmental Safety, 289, 117494.

Datta, A., Mishra, S., Manna, K., Saha, K. D., Mukherjee, S., & Roy, S. (2020). Pro-oxidant therapeutic activities of cerium oxide nanoparticles in colorectal carcinoma cells. ACS Omega, 5(17), 9714–9723.

Demir, E., Demir, F. T., & Marcos, R. (2022). Drosophila as a suitable in vivo model in the safety assessment of nanomaterials. Advances in Experimental Medicine and Biology, 1357, 275–301.

Doan, V. C. (2025). Rare earth elements in agroecosystems: A review of plant defenses and cascading effects on insect herbivores and pollinators. Journal of Plant Interactions, 20(1), 2581395.

Elqady, E. M., El-said, E., Tharwat, A. A., Abou El-Khashab, L. A., Mostafa, I. M. Y., Hamed, F. Z., Morsi, W. M., Rezk, M. M., & Abou El-Enain, I. M. (2025). Biogenic synthesis of titanium nanoparticles by Streptomyces rubrolavendulae for sustainable management of Icerya aegyptiaca (Douglas). Scientific Reports, 15, 1380.

El-Samad, L. M., Bakr, N. R., Abouzid, M., El-Samad, M. F., El-Samad, M. A., El-Samad, A. M., & El-Samad, A. A. (2024). Nanoparticles-mediated entomotoxicology: Lessons from biologica. Ecotoxicology, 33, 305–324.

El-Sayied Ali, S., El-Ghannam, G., Hashish, M. E. S., El-Sayied, A., El-Mahdy, R., & El-Sheikh, M. (2024). Exploring bee venom and silver nanoparticles for controlling foulbrood pathogen and enhancing lifespan of honeybees. Scientific Reports, 14, 19013.

Faisal, S., Jan, H., Shah, S. A., Shah, S., Khan, A., Akbar, M. T., Rizwan, M., Jan, F., Akhtar, N., Khattak, A., & Syed, S. (2021). Green synthesis of zinc oxide (ZnO) nanoparticles using aqueous fruit extracts of Myristica fragrans: Their characterizations and biological and environmental applications. ACS Omega, 6(14), 9709–9722.

Filho, W., Kotter, R., Özuyar, P., Abubakar, I., Eustachio, J., Matandirotya, N. (2023). Understanding rare earth elements as critical raw materials. Sustainability, 15(3), 1919.

Flamminii, F., Consalvo, A., Cichelli, A., & Chiaudani, A. (2024). Assessing mineral content and heavy metal exposure in Abruzzo honey and bee pollen from different anthropic areas. Foods, 13(12), 1930.

Formicki, G., Greń, A., Stawarz, R., Zyśk, B., & Gał, A. (2013). Metal content in honey, propolis, wax, and bee pollen and implications for metal pollution monitoring. Polish Journal of Environmental Studies, 22, 99–106.

Gałczyńska, M., Gamrat, R., Bosiacki, M., Sotek, Z., Stasińska, M., & Ochmian, I. (2021). Micro and macroelements in honey and atmospheric pollution (NW and Central Poland). Resources, 10(8), 86.

Gunasekaran, N. K., Nazario Bayon, N., Tumkur, P. P., Prabhakaran, K., Hall, J. C., & Ramesh, G. T. (2025). Anticancer activity of cerium oxide nanoparticles towards human lung cancer cells. Nanomanufacturing, 5(2), 6.

Haas, J., Zaworra, M., Glaubitz, J., Hertlein, G., Kohler, M., Lagojda, A., Lueke, B., Maus, C., Almanza, M. T., Davies, T. G. E., Bass, C., & Nauen, R. (2021). A toxicogenomics approach reveals characteristics supporting the honey bee (Apis mellifera L.) safety profile of the butenolide insecticide flupyradifurone. Ecotoxicology and Environmental Safety, 217, 112247.

Hawthorne, J., De la Torre Roche, R., Xing, B., Newman, L. A., Ma, X., Majumdar, S., Gardea-Torresdey, J., & White, J. C. (2014). Particle-size dependent accumulation and trophic transfer of cerium oxide through a terrestrial food chain. Environmental Science and Technology, 48(22), 13102–13109.

Höllriegl, V., González-Estecha, M., Trasobares, E. M., Giussani, A., Oeh, U., Herraiz, M. A., & Michalke, B. (2010). Measurement of cerium in human breast milk and blood samples. Journal of Trace Elements in Medicine and Biology, 24(3), 193–199.

Iskander, F. (1995). Trace and minor elements in four commercial honey brands. Journal of Radioanalytical and Nuclear Chemistry, 201(5), 401–408.

Kaur, I. P., Bhandari, R., Bhandari, S., & Kakkar, V. (2014). Issues and concerns in nanotech product development and its commercialization. Journal of Controlled Release, 193, 51–62.

Khalifa, S. A. M., Elshafiey, E. H., Shetaia, A. A., El-Wahed, A. A. A., Algethami, A. F., Musharraf, S. G., AlAjmi, M. F., Zhao, C., Masry, S. H. D., Abdel-Daim, M. M., Halabi, M. F., Kai, G., Al Naggar, Y., Bishr, M., Diab, M. A. M., & El-Seedi, H. R. (2021). Overview of bee pollination and its economic value for crop production. Insects, 12(8), 688.

Khalifa, S. A. M., Shetaia, A. A., Eid, N., Abd El-Wahed, A. A., Abolibda, T. Z., El Omri, A., Yu, Q., Shenashen, M. A., Hussain, H., Salem, M. F., Guo, Z., Alanazi, A. M., & El-Seedi, H. R. (2024). Green innovation and synthesis of honeybee products-mediated nanoparticles: potential approaches and wide applications. Bioengineering, 11(8), 829.

Khan, Y., Ullah, N., Khan, A., Alotaibi, S. H., Alshammari, F. H., Alshammari, B. A., & Alshammari, N. A. (2022). Classification, synthetic, and characterization approaches to nanoparticles, and their applications in various fields of nanotechnology: A review. Catalysts, 12(11), 1386.

Kos, M., Jemec Kokalj, A., Glavan, G., Marolt, G., Zidar, P., Božič, J., Novak, S., & Drobne, D. (2017). Cerium (IV) oxide nanoparticles induce sublethal changes in honeybees after chronic exposure. Environmental Science: Nano, 4(1), 240–247.

Labsvards, K. D., Rudovica, V., Borisova, A., Kokina, K., Bertins, M., Naumenko, J., & Viksna, A. (2023). Multi-element profile characterization of monofloral and polyfloral honey from Latvia. Foods, 12(22), 4091.

Leska, A., Nowak, A., Nowak, I., & Górczyńska, A. (2021). Effects of insecticides and microbiological contaminants on Apis mellifera health. Molecules, 26(16), 5080.

Li, J., Mu, Q., Du, Y., Luo, J., Liu, Y., & Li, T. (2020). Growth and photosynthetic inhibition of cerium oxide nanoparticles on soybean (Glycine max). Bulletin of Environmental Contamination and Toxicology, 105(1), 119–126.

Ligor, M., Kowalkowski, T., & Buszewski, B. (2022). Comparative study of the potentially toxic elements and essential microelements in honey depending on the geographic origin. Molecules, 27(17), 5474.

Liu, Y. J., Jing, Z., Bai, X. T., Diao, Q. Y., Wang, J., Wu, Y. Y., Zhao, Q., Xia, T., Xing, B., Holden, P. A., & Ge, Y. (2021). Nano-La2O3 induces honeybee (Apis mellifera) death and enriches for pathogens in honeybee gut bacterial communities. Frontiers in Microbiology, 12, 780943.

Ma, Y., Yao, Y., Yang, J., He, X., Ding, Y., Zhang, P., Zhang, J., Wang, G., Xie, C., Luo, W., Zhang, J., Zheng, L., Chai, Z., Zhao, Y., & Zhang, Z. (2018). Trophic transfer and transformation of CeO2 nanoparticles along a terrestrial food chain: Influence of exposure routes. Environmental Science and Technology, 52(14), 7921–7927.

Magdas, A. A., Guyon, F., Puscas, R., Vigouroux, A., Gaillard, L., Dehelean, A., Feher, I., & Cristea, G. (2021). Applications of emerging stable isotopes and elemental markers for geographical and varietal recognition of Romanian and French honeys. Food Chemistry, 334, 127599.

Mair, K. S., Irrgeher, J., & Haluza, D. (2023). Elucidating the role of honey bees as biomonitors in environmental health research. Insects, 14(11), 874.

Majumdar, S., Trujillo-Reyes, J., Hernandez-Viezcas, J. A., White, J. C., Peralta-Videa, J. R., & Gardea-Torresdey, J. L. (2016). Cerium biomagnification in a terrestrial food chain: Influence of particle size and growth stage. Environmental Science and Technology, 50(13), 6782–6792.

Mamatha, M. G., Ansari, M. A., Begum, M. Y., Prasad, B. D., Al Fatease, A., Hani, U., Alomary, M. N., Sultana, S., Punekar, S. M., Nivedika, M. B., Lakshmeesha, T. R., & Ravikiran, T. (2024). Green synthesis of cerium oxide nanoparticles, characterization, and their neuroprotective effect on hydrogen peroxide-induced oxidative injury in human neuroblastoma (SH-SY5Y) cell line. ACS Omega, 9(2), 2639–2649.

Mărgăoan, R., Topal, E., Balkanska, R., Yücel, B., Oravecz, T., Cornea-Cipcigan, M., & Vodnar, D. C. (2021). Monofloral honeys as a potential source of natural antioxidants, minerals and medicine. Antioxidants, 10(7), 1023.

Matuszewska, E., Klupczynska, A., Maciołek, K., Kokot, Z. J., & Matysiak, J. (2021). Multielemental analysis of bee pollen, propolis, and royal jelly collected in West-Central Poland. Molecules, 26(9), 2415.

Mishra, M., & Panda, M. (2021). Reactive oxygen species: The root cause of nanoparticle-induced toxicity in Drosophila melanogaster. Free Radical Research, 55(6), 671–687.

Naccari, C., Ferrantelli, V., Cammilleri, G., Barbaccia, G., Riolo, P., Ferrante, M. C., Procopio, A., & Palma, E. (2025). Study of toxic metals and microelements in honey as a tool to support beekeeping production and consumer safety. Foods, 14(11), 1986.

Omelchun, Y. A., Kobish, A. I., Klochkova, N. P., & Shevchenko, L. V. (2022). Validation of the multiresidue method analysis for pesticides in bee honey by UPLC-MS/MS using the method of samples preparation QuEChERS. Methods and Objects of Chemical Analysis, 17(3), 141–152.

Omelchun, Y. A., Shevchenko, L. V., Nikitina, L. M., Solomon, V. V., Mykhalska, V. M., Furman, S. V., Lisohurska, D. V., Lisohurska, O. V. (2025a). Pesticides as a cause of honeybee (Apis mellifera) mortality and their persistence in honey. Biosystems Diversity, 33(1), e2501.

Omelchun, Y. A., Shevchenko, L. V., Nikitina, L. M., Solomon, V. V., Voynalovich, M. V., Mykhalska, V. M., Zlamanyuk, L. M., Busol, L. M. (2025b). Accumulation of a multi-component mixture of pesticides in soil, plants, bee organisms, and beekeeping products. Biosystems Diversity, 33(1), e2503.

Omelchun, Y., Shevchenko, L., Voynalovich, M., Savchenko, O., Hryshchenco, N., Tkach, G., Androshchuk, O., Drachuk, O., Kozii, M., Rzhevskyi, H., & Slyva, Y. (2023). Effects of pesticides on bee populations and safety of bee honey in Ukraine. Potravinarstvo Slovak Journal of Food Sciences, 17, 801–815.

Parimi, D., Sundararajan, V., Sadak, O., Gunasekaran, S., Sheik Mohideen, S., & Sundaramurthy, A. (2019). Synthesis of positively and negatively charged CeO₂ nanoparticles: Investigation of the role of surface charge on growth and development of Drosophila melanogaster. ACS Omega, 4(1), 104–113.

Pasias, I. N., Kiriakou, I. K., & Proestos, C. (2017). HMF and diastase activity in honeys: A fully validated approach and a chemometric analysis for identification of honey freshness and adulteration. Food Chemistry, 229, 425–431.

Peters, R. J. B., Bouwmeester, H., Gottardo, S., Amenta, V., Arena, M., Brandhoff, P., Marvin, H. J. P., Mech, A., Moniz, F. B., Qasim, K., Schoonjans, R., & Vettori, M. V. (2016). Nanomaterials for products and application in agriculture, feed and food. Trends in Food Science and Technology, 54, 155–164.

Priscilla, S., Venkatasubbu, G., & Sheik Mohideen, S. (2025). Chitosan-coated titanium dioxide nanoparticles: Fabrication, characterisation and toxicological evaluation in Drosophila melanogaster. Nanotechnology for Environmental Engineering, 10, 20.

Puscion-Jakubik, A., Borawska, M., & Socha, K. (2020). Modern methods for assessing the quality of bee honey and botanical origin identification. Foods, 9, 1028.

Sarnatskaya, V., Shcherbakov, A., Ivanov, V., Shcherbakova, O., Popov, A., Popova, N., Ivanova, O., & Baranchikov, A. (2020). Biological activity of cerium dioxide nanoparticles. Journal of Biomedical Materials Research Part A, 108(8), 1703–1712.

Schuhmann, A., Schmid, A. P., Manzer, S., Schulte, J., & Scheiner, R. (2022). Interaction of insecticides and fungicides in bees. Frontiers in Insect Science, 1, 808335.

Sofranko, A., Wahle, T., Kolling, J., Heusinkveld, H. J., Stahlmecke, B., Rosenbruch, M., Albrecht, C., & Schins, R. P. F. (2022). Effects of subchronic dietary exposure to the engineered nanomaterials SiO2 and CeO2 in C57BL/6J and 5xFAD Alzheimer model mice. Particle and Fibre Toxicology, 19(1), 23.

Sundararajan, V., Venkatasubbu, G. D., & Sheik Mohideen, S. (2021). Investigation of therapeutic potential of cerium oxide nanoparticles in Alzheimer's disease using transgenic Drosophila. 3 Biotech, 11(4), 159.

Tonk-Rügen, M., Vilcinskas, A., & Wagner, A. E. (2022). Insect models in nutrition research. Biomolecules, 12(11), 1668.

Tourinho, P. S., Waalewijn-Kool, P. L., Zantkuijl, I., Jurkschat, K., Svendsen, C., Soares, A. M., Loureiro, S., & van Gestel, C. A. (2015). CeO2 nanoparticles induce no changes in phenanthrene toxicity to the soil organisms Porcellionides pruinosus and Folsomia candida. Ecotoxicology and Environmental Safety, 113, 201–206.

Tripathi, S., Mahra, S. J. V., Tiwari, K., Rana, S., Tripathi, D. K., Sharma, S., & Sahi, S. (2023). Recent advances and perspectives of nanomaterials in agricultural management and associated environmental risk: A review. Nanomaterials, 13(10), 1604.

Ullah, R., Jan, F. A., Gulab, H., Muhammad, A., Ali, S., Ahmad, S., Khan, A., & Shah, J. (2022). Metals contents in honey, beeswax and bees and human health risk assessment due to consumption of honey: A case study from selected districts in Khyber Pakhtunkhwa, Pakistan. Archives of Environmental Contamination and Toxicology, 82(3), 341–354.

Vit, P., Araque, M., Chuttong, B., Moreno, E., Contreras, R. R., Wang, Q., Wang, Z., Betta, E., & Bankova, V. (2024). Pot-pollen volatiles, bioactivity, synergism with antibiotics, and bibliometrics overview, including direct injection in food flavor. Foods, 13(23), 3879.

Voitsitskiy, V. M., Danchuk, V. V., Ushkalov, V. O., Midyk, S. V., Kepple, O. Y., Danchuk, О. V., & Shevchenko, L. V. (2019). Migration of antibiotics residual quantities in aquatic ecosystems. Ukrainian Journal of Ecology, 9(3), 280–286.

Wang, Y., Ma, C., Dang, F., Zhao, L., Zhou, D., & Gu, X. (2024). Mixed effects and co-transfer of CeO2 NPs and arsenic in the pakchoi-snail food chain. Journal of Hazardous Materials, 462, 132770.

Wojtczak, I., Brzozowska, W., Trykowski, G., & Sprynskyy, M. (2024). Diatom biosilica functionalised with metabolically deposited cerium oxide nanoparticles. Materials, 17(10), 2390.

Zafeiraki, E., Sabo, R., Kasiotis, K. M., Machera, K., Sabová, L., & Majchrák, T. (2022). Adult honeybees and beeswax as indicators of trace elements pollution in a vulnerable environment: Distribution among different apicultural compartments. Molecules, 27(19), 6629.

Zavrtnik, S., Loborec, J., Kapelj, S., & Grčić, I. (2024). Environmental biomonitoring of heavy and toxic metals using honeybees and their products – an overview of previous research. Sustainability, 16(19), 8526.

Zhang, Y., Sun, W., Wang, M., Qian, Y., Zheng, Q., Wang, W., Yang, H., Wang, Y., Zhou, M., Wang, X., & Yang, C. (2025). Application of nanoparticles in the treatment of acute lung injury: Current situation and future directions. Materials Today. Bio, 34, 102199.

Zhou, X., El-Sappah, A. H., Khaskhoussi, A., Huang, Q., Atif, A. M., Elhamid, M. A. A., Ihtisham, M., El-Maati, M. F. A., Soaud, S. A., & Tahri, W. (2025). Nanoparticles: A promising tool against environmental stress in plants. Frontiers in Plant Science, 15, 1509047.

Published
2026-01-16
How to Cite
Nikitina, L. M., Zasekin, D. A., Shevchenko, L. V., Zholobak, N. M., Postoenko, V. O., Andrusyshyna, I. M., Morfin, N., Grushanska, N. H., Yefimenko, T. M., Odnosum, H. V., & Postoenko, H. V. (2026). Effect of feeding honey bees Apis mellifera with nanocerium dioxide on the mineral composition of honey, wax and the bees’ bodies. Regulatory Mechanisms in Biosystems, 17(1), e26002. https://doi.org/10.15421/0226002

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