Original Scientific Article
Active role of lactoferrin on arsenic and imidacloprid toxicity in broiler chicks
Marwa Fouad Hassan ,
Asmaa Gamal Abd El Monsef ,
Nermin Farouq El Zohairy ,
Sanaa Mohamed Salem ,
Safaa Mohamed Elmesalamy ,
Hamada Mahmoud Yousif * ,
Mogda Kamel Mansour

Mac Vet Rev 2024; 47 (2): 167 - 178

doi.org/10.2478/macvetrev-2024-0028

Received: 10 May 2024

Received in revised form: 25 August 2024

Accepted: 26 August 2024

Available Online First: 02 October 2024

Published on: 15 October 2024

Correspondence: Hamada Mahmoud Yousif, hamadayousif82@gmail.com
PDF HTML

Abstract

This work aimed to evaluate the lactoferrin (LF) effect on arsenic (As) and imidacloprid (IMI) toxicity in broiler chicks. One-week old broiler chicks (n=105) were divided into seven groups (x15 each). The animals were orally supplemented with As, IMI, and/or LF for 4 weeks as follows: Control (G1) no supplements, G2 supplemented with As, G3 supplemented with IMI, G4 supplemented with As+IMI, G5 supplemented with As+LF, G6 supplemented with IMI+LF, G7 supplemented with As+IMI+LF. Body weight and weight gain were recorded on weekly interval. Blood, serum, liver, kidney, and muscle samples were collected at the end of the experimental period for biochemical and histopathological examination. Body weight performance, hematological, serum, and liver tissue biochemical analysis revealed adverse changes in G2, G3, and G4 compared to control, G5, G6, and G7. There was higher tissue residue of As and IMI in G4 compared to G5, G6, and G7. Liver histopathological changes in the groups supplemented with As and/or IMI were observed with necrosis, congestion, and inflammatory cell aggregates. The use of LF in broiler chicks improves weight gain performance and modulates the adverse effects of As and/or IMI toxicity.

Keywords: lactoferrin effect, arsenic toxicity, imidacloprid toxicity, histopathology, broilers chicks

References

1. Valskys, V., Hassan, H.R., Wołkowicz, S., Satkūnas, J., Kibirkštis, G., Ignatavičius, G. (2022). A review on detection techniques, health hazards and human health risk assessment of arsenic pollution in soil and groundwater. Minerals 12(10): 1326. https://doi.org/10.3390/min12101326 
2. Paswan, S., Niyogi, D., Choudhary, P.K., Raghubanshi, D. (2018). Ameliorating effect of ascorbic acid on clinicopathological changes of induced sub-acute arsenic toxicity in broiler birds. Int J Curr Microbiol App Sci. Special Issue 7, 5084-5094.
3. Ahmad, S., Kitchin, K.T., Cullen, W.R. (2000). Arsenic species that cause release of iron from ferritin and generation of activated oxygen. Arch Biochem Biophys. 382(2): 195-202. https://doi.org/10.1006/abbi.2000.2023 PMid:11068869
4. Ford, M. (2002). Arsenic. In: L.R. Goldfrank, N. Flomnbaum, N. Lewin, M.A. Howland, R. Hoffman, L. Nelson (Eds.), Goldfrank’s Toxicological Emergencies, 7th Ed. (pp. 1183-1195). New York, USA: McGraw-Hill
5. Craddock, H.A., Huang, D., Turner, P.C., Quirós-Alcalá, L., Payne-Sturges, D.C. (2019). Trends in neonicotinoid pesticide residues in food and water in the United States, 1999-2015. Environ Health 18, 7. https://doi.org/10.1186/s12940-018-0441-7 PMid:30634980 PMCid:PMC6330495
6. Thompson, D.A., Lehmler, H.J., Kolpin, D.W., Hladik, M.L., Vargo, J.D., Schilling, K.E., Le-Fevre, G.H., et al. (2020). A critical review on the potential impacts of neonicotinoid insecticide use: current knowledge of environmental fate, toxicity, and implications for human health. Environ Sci Processes Impacts. 22, 1315-1346. https://doi.org/10.1039/C9EM00586B PMid:32267911
7. Lv, Y., Bing, Q., Lv, Z., Xue, J., Li, S., Han, B., Yang, Q., et al. (2020). Imidacloprid-induced liver fibrosis in quails via activation of the TGF-β1/Smad pathway. Sci Total Environ. 705, 135915. https://doi.org/10.1016/j.scitotenv.2019.135915 PMid:31835194
8. Wang, X., Anadón, A., Wu, Q., Qiao, F., Ares, I., Martínez-Larrañaga, M.R., Yuan, Z., Martínez, M.A. (2018). Mechanism of neonicotinoid toxicity: impact on oxidative stress and metabolism. Ann Rev Pharmacol Toxicol. 58, 471-507. https://doi.org/10.1146/annurev-pharmtox-010617-052429 PMid:28968193
9. Ravikanth, V., Lakshman, M., Madhuri, D., Kalakumar, B. (2018). Effect of spinosad and imidacloprid on serum biochemical alterations in male broilers and its amelioration with vitamin E and silymarin. Int J Curr Microbiol App Sci. 7(4): 2186-2192. https://doi.org/10.20546/ijcmas.2018.704.248 
10. Mahajan, L., Verma, P.K., Raina, R., Sood, S. (2018). Toxic effects of imidacloprid combined with arsenic: oxidative stress in rat liver. Toxicol Ind Health. 34(10): 726-735. https://doi.org/10.1177/0748233718778993 PMid:30033815
11. Vega-Bautista, A., de la Garza, M., Carrero, J.C., Campos-Rodríguez, R., Godínez-Victoria, M., Drago-Serrano, M.E. (2019). The impact of lactoferrin on the growth of intestinal inhabitant bacteria. Int J Mol Sci. 20(19): 4707. https://doi.org/10.3390/ijms20194707 PMid:31547574 PMCid:PMC6801499
12. Olyayee, M., Javanmard, A., Janmohammadi, H., Kianfar, R., Alijani, S., Ghelenj, S.A.M. (2023). Supplementation of broiler chicken diets with bovine lactoferrin improves growth performance, histological parameters of jejunum and immune-related gene expression. J Anim Physiol Anim Nutr. 107(1): 200-213. https://doi.org/10.1111/jpn.13683 PMid:35102621
13. Kell, D.B., Heyden, E.L., Pretorius, E. (2020). The biology of lactoferrin, an iron-binding protein that can help defend against viruses and bacteria. Front Immunol. 11, 1221. https://doi.org/10.3389/fimmu.2020.01221 PMid:32574271 PMCid:PMC7271924
14. Legrand, D., Elass, E., Carpentier, M., Mazurier, M. (2005). Lactoferrin: a modulator of immune and inflammatory responses. Cell Mol Life Sci. 62, 2549. https://doi.org/10.1007/s00018-005-5370-2 PMid:16261255 PMCid:PMC7079806
15. Abd El Monsef, A.G., El Zohairy, N.F., Hassan, M.F., Salem, S.M., Gouda, A.A., Mansour, M.K., Alkhaldi, A.A.M., et al. (2024). Effects of prebiotic (lactoferrin) and diclazuril on broiler chickens experimentally infected with Eimeria tenella. Front Vet Sci. 11, 1416459. https://doi.org/10.3389/fvets.2024.1416459 PMid:39036795 PMCid:PMC11258017
16. Inns, R.H., Bright, J.E., Marrs, T.C. (1988). Comparative acute systemic toxicity of sodium arsenite and dichloro (2~hlorovinyl) arsine in rabbits. Toxicology 51(2-3): 213-222. https://doi.org/10.1016/0300-483X(88)90151-5 PMid:3176029
17. Kammon, A.M., Brar, R.S., Banga, H.S., Sodhi, S. (2012). Ameliorating effects of vitamin E and selenium on immunological alterations induced by imidacloprid chronic toxicity in chickens. J Environ Anal Toxicol. S4. https://doi.org/10.4172/2161-0525.S4-007 
18. Enany, M.E., Algammal, A.M., Solimane, R.T., El-Sissi, A.F., Hebashy, A.A. (2017). Evaluation of lactoferrin immunomodulatory effect on the immune response of broiler chickens. SCVMJ 22(1): 135-146. https://doi.org/10.21608/scvmj.2017.62452 
19. Uluozlu, O.D., Tuzen, M., Mendil, D., Soylak, M. (2009). Assessment of trace element contents of chicken products from turkey. J Hazard Mater. 163(2-3): 982-987. https://doi.org/10.1016/j.jhazmat.2008.07.050 PMid:18752893
20. Dewangan, G., Patra, P.H., Mishra, A., Singh, A.K., Dutta, B.K., Sar, T.K., Chakraborty, A.K., Mandal, T.K. (2012). Haemobiochemical, immunological, antioxidant status and residues of flumethrin following weekly dermal application in goats. Toxicol Environ Chem. 94(2): 377-387. https://doi.org/10.1080/02772248.2011.641968 
21. Suvarna, K.S., Layton, C., Bancroft, J.D. (2018). Bancroft’s theory and practice of histological techniques, 8th Ed. Netherlands: E-Book, Elsevier Health Sciences
22. Feldman, B.F., Zinkl, J.G., Jain, N.C. (2000). Schalm’s veterinary hematology. 5th Ed. Canada: Lippincott Williams and Wilkins
23. Anderson, C.B., Latimer, R.S. (1990). Cyto-chemical staining characteristics of chickens heterophils and eosinophils. Vet Clin Pathol. 19(2): 51-54. https://doi.org/10.1111/j.1939-165X.1990.tb00543.x PMid:12684938
24. Davis, B. (1964). Disk electrophoresis - II Method and application to human serum protein. Ann N Y Acad Sci. 121(2): 404-427. https://doi.org/10.1111/j.1749-6632.1964.tb14213.x PMid:14240539
25. Pang, S., Han, B., Wu, P., Yang, X., Liu, Y., Li, J., Lv, Z., Zhang, Z. (2024). Resveratrol alleviates inorganic arsenic-induced ferroptosis in chicken brain via activation of the Nrf2 signaling pathway. Pestic Biochem Physiol. 201, 105885. https://doi.org/10.1016/j.pestbp.2024.105885 PMid:38685251
26. Eleiwa, N.Z., El-Shabrawi, A.A., Ibrahim, D., Abdelwarith, A.A., Younis, E.M., Davies, S.J., Metwally, M.M.M., Abu-Zeid, E.H. (2023). Dietary curcumin modulating effect on performance, antioxidant status, and immune-related response of broiler chickens exposed to imidacloprid insecticide. Animals 13(23): 3650. https://doi.org/10.3390/ani13233650 PMid:38067001 PMCid:PMC10705146
27. Kawakami, H., Hiratsuka, M., Dosako, S. (1988). Effects of iron-saturated lactoferrin on iron absorption. Agric Biol Chem. 52(4): 903-908. https://doi.org/10.1080/00021369.1988.10868784 
28. Duker, A., Carranza, E., Hale, M. (2005) Arsenic geochemistry and health. Environ Int. 31(5): 631-641. https://doi.org/10.1016/j.envint.2004.10.020 PMid:15910959
29. Khandia, R., Pathe, C.S., Vishwakarma, P., Dhama, K., Munjal, A. (2020). Evaluation of the ameliorative effects of Phyllanthus niruri on the deleterious insecticide imidacloprid in the vital organs of chicken embryos. J Ayurveda Integ Med. 11(4): 495-501. https://doi.org/10.1016/j.jaim.2019.03.003 PMid:31757597 PMCid:PMC7772494
30. Conte, F.M., Cestonaro, L.V., Piton, Y.V., Guimaraes, N., Garcia, S.C., da Silva, D., Arbo, M.D. (2022). Toxicity of pesticides widely applied on soybean cultivation: synergistic effects of fipronil, glyphosate and imidacloprid in HepG2 cells. Toxicol In Vitro 84, 105446. https://doi.org/10.1016/j.tiv.2022.105446 PMid:35850439
31. Abdel-Hameid, N.A.H. (2009). A protective effect of calcium carbonate against arsenic toxicity of the Nile catfish (Clarias gariepinus). Turk J Fish Aquat Sci. 9(2): 191-200.
32. Arfat, Y., Mahmood, N., Tahir, M.U., Rashid, M., Anjum, S., Zhao, F., Li, D.J., et al. (2014). Effect of imidacloprid on hepatotoxicity and nephrotoxicity in male albino mice. Toxicol Rep. 1, 554-561. https://doi.org/10.1016/j.toxrep.2014.08.004 PMid:28962268 PMCid:PMC5598541
33. Eid, Y.Z., Omara, Y., Ragab, A., Ismail, A., Zommara, M., Dawood, M.A.O. (2023). Mitigation of Imidacloprid Toxicity in Poultry Chicken by Selenium Nanoparticles, Growth Performance, Lipid Peroxidation, and Blood Traits. Biol Trace Elem Res. 201, 5379-5388. https://doi.org/10.1007/s12011-023-03592-5 PMid:36790585 PMCid:PMC10509070
34. Li, J., Guo, C., Liu, Y., Han, B., Lv, Z., Jiang, H., Li, S., Zhang, Z. (2024). Chronic arsenic exposureprovoked biotoxicity involved in liver-microbiotagut axis disruption in chickens based on multi-omics technologies. J Adv Res. S2090-1232(24)00032-8. https://doi.org/10.1016/j.jare.2024.01.019 
35. Wang, Y.H., Wang, Y.Q., Yu, X.G., Lin, Y., Liu, J.X., Wang, W.Y., Yan, C.H. (2023). Chronic environmental inorganic arsenic exposure causes social behavioral changes in juvenile zebra fish (Danio rerio). Sci Total Environ. 867, 161296. https://doi.org/10.1016/j.scitotenv.2022.161296 PMid:36592900
36. Aggarwal, M., Naraharisetti, S.B., Sarkar, S.N., Rao, G.S., Degen, G.H., Malik, J.K. (2009). Effects of subchronic coexposure to arsenic and endosulfan on the erythrocytes of broiler chickens: a biochemical study. Arch Environ Contam Toxicol. 56(1): 139-148. https://doi.org/10.1007/s00244-008-9171-0 PMid:18443843
37. Johnson, W.M., Wilson-Delfosse, A.L., Mieyal, J.J. (2012). Dysregulation of glutathione homeostasis in neurodegenerative diseases. Nutrients 4(10): 1399-1440. https://doi.org/10.3390/nu4101399 PMid:23201762 PMCid:PMC3497002
38. Sattar, A., Khan, A., Hussain, H.I., He, C., Hussain, R., Zhiqiang, S., Saleemi, M.K., Gul, S.T. (2016). Immunosuppressive effects of arsenic in broiler chicks exposed to Newcastle disease virus. J Immunotoxicol. 13(6): 861-869. https://doi.org/10.1080/1547691X.2016.1217105 PMid:27687888
39. Roy, C.L., Jankowski, M.D., Ponder, J., Chen, D. (2020). Sublethal and lethal methods to detect recent imidacloprid exposure in birds with application to field studies. Environ Toxicol Chem. 39(7): 1355-1366. https://doi.org/10.1002/etc.4721 PMid:32274821 PMCid:PMC8164728
40. Ahmed, S., Siddiqui, M.S.I., Islam, K., Islam, M.N., Gani, M.U., Moonmoon, S., Rashid, M.H., Awal, M.A. (2016). Arsenic deposition in different organs or tissues in an experimental toxicosis of White New-Zealand Rabbit. Asian J Med Biol Res. 2(3): 422-428. https://doi.org/10.3329/ajmbr.v2i3.30113 

Copyright

© 2024 Hassan M.F. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Conflict of Interest Statement

The authors declared that they have no potential lict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 47, Issue 2, Pages 167-178, e-ISSN 1857-7415, p-ISSN 1409-7621, DOI: 10.2478/macvetrev-2024-0028

The all content of the Macedonian Veterinary Review, except where otherwise noted, is licensed under a Creative Commons Attribution License.