Juglans regia Kernel Powder Supplementation in Broiler Chickens Fed Aflatoxin-Contaminated Diets: Effect on Growth, Serum Chemistry Indices, Immunoglobulin and Pro-Inflammatory Cytokines

Document Type : Original Research

Authors
1 Department of Animal Science, Adekunle Ajasin University, Akungba Akoko, Nigeria.
2 Department of Agricultural Technology, The Federal Polytechnic, Ado Ekiti, Nigeria.
3 Department of Animal Health and Production Technology, Federal College of Agriculture, Akure, Nigeria.
4 Department of Animal Production and Health, The Federal University of Technology, Akure, Nigeria.
5 Department of Medical Laboratory Science, University of Medical Sciences, Ondo City, Nigeria.
Abstract
This study aimed to investigate the impact of Juglans regia Kernel Powder (JKP) on broiler chickens subjected to Aflatoxin (AF)-contaminated diets during a 42-day feeding trial conducted in February and March 2022. A total of 240 one-day-old broiler chickens were divided into four dietary groups: Diet 1 (Control), Diet 2 (0.5 mg kg-1 AF), Diet 3 (0.5 mg kg-1 AF+250 mg kg-1 JKP), and Diet 4 (0.5 mg kg-1 AF+500 mg kg-1 JKP). Birds on Diet 2 exhibited a significantly lower (P= 0.01) relative growth rate compared to the other diets. JKP supplementation at 250 mg kg-1 (Diet 3) and 500 mg kg-1 (Diet 4) mitigated the negative impact of AF on growth. Birds on Diet 2 showed significantly lower (P= 0.01) serum concentrations of total protein, albumin, and globulin compared to those on Diets 1, 3, and 4. Elevated levels of Aspartate aminotransferase (AST) and creatinine in Diet 2 indicated liver and kidney damage. Alanine Transaminase (ALT) concentrations in Diet 2 were higher (P= 0.01) than Diets 1 and 4. Birds fed diet 2 had lower glucose levels (P= 0.01) than diets 1 and 4. IgA levels in birds fed Diet 2 were lower (P= 0.03) than those in the birds fed Diet 4. Birds fed diet 2 had considerably (P< 0.05) lower IgE and IgG levels than birds fed diets 1 and 4. Nuclear Factor Kappa B (NFK B) was higher (P= 0.01) in birds fed Diet 2 compared to other diets. Interleukin 6 (IL 6) concentration was significantly (P= 0.01) higher in the birds fed Diet 2 than in the other diets. A recommended dietary supplementation of 250 mg kg-1 JKP is suggested based on the observed ameliorative effects.

Keywords


1. Aboelhassan, D.M., Hafiz, N.A., Darwish, H.R., Shabana, M.E., Eshak, M.G., Hassanane, M.M., Farag, I.M., and Abdalla, A.M. (2018). Enhancing effects of Moringa oleifera leaf extract on carcinogenic Aflatoxin B1-induced genetic alterations, haematoxicity and histological changes in liver and kidney of rats. Bioscience Research, 15(2), 814-833.
2. Adebayo, F.B., Adu, O.A., Chineke, C.A., Oloruntola, O.D., Omoleye, O.S., Adeyeye, S.A., and Ayodele, S.O. (2020). The performance and heamatological indices of broiler chickens fed Chromium Picolinate and vitamin C supplemented diets. Asian Journal of Research in Animal and Veterinary Science, 6(4), 54-61.
3. Adegbeye, M.J., Oloruntola, O.D., Asaniyan, E.K., Agunbiade, B., Oisagah, E.A. and Ayodele, S.O. (2020). Pawpaw, Black Cumin, and Mustard Seed Meals Dietary Supplementation in Broiler Chickens: Effect on Performance, Gut Microflora, and Gut Morphology, Journal of Agricultural Science and Technology, 22(5): 1235-1246.
4. Alpsoy, L. and Yalvac, M.E. (2011). Key roles of vitamins A, C, and E in aflatoxin B1-induced oxidative stress. Vitamins and Hormones, 86, 287-305.
5. An, Y., Shi, X., Tang, X., Wang, Y., Shen, F., Zhang, Q., Wang, C., Jiang, M., Liu, M., and Yu, L (2017). Aflatoxin B1 Induces Reactive Oxygen Species-Mediated Autophagy and Extracellular Trap Formation in Macrophages. Frontiers of Cell and Infectious Microbiology, 7, 53. doi: 10.3389/fcimb.2017.00053
6. AOAC. (2010). Official method of analysis, 18th edition. Association of Official Analytical Chemists, Washington D.C.
7. Baiano, A., and del Nobile, M.A. (2015). Antioxidant compounds from vegetable matrices: Biosynthesis, occurrence, and extraction systems. Critical Reviews in Food Science and Nutrition, 56, 2053–2068. doi: 10.1080/10408398.2013.812059.
8. Basmacioglu, H., Oguz, H., Ergul, M., Col, R., and Birdane, Y.O. (2005). Effect of dietary esterified glucomannan on performance, serum biochemistry and haematology in broilers exposed to aflatoxin. Czech Journal of Animal Science, 50, 2005 (1): 31–39.
9. Bhat, A. A., Shakeel, A., Rafiq, S., Farooq, I., Malik, A. Q., Alghuthami, M. E., Alharthi, S., Qanash, H., and Alharthy, S. A. (2023). Juglans regia Linn.: A Natural Repository of Vital Phytochemical and Pharmacological Compounds. Life (Basel, Switzerland), 13(2), 380. https://doi.org/10.3390/life13020380
10. Burel, S.D., Favrot, M.C., Fremy, J.M., Massimi, C., Prigent, P., Debongnie, L.P. and Morgavi, D. (2009). Review of mycotoxin-detoxifying agents used as feed additives: mode of action, efficacy and feed/food safety. EFSA-Q- pp.2009-00839, EFSA J, Dec 82012; 2012:564367. doi: 10.1100/2012/564367.
11. Cai, Y.Z., Luo, Q., Sun, M., and Corke, H. (2004). Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Science, 74, 2157–2184. doi: 10.1016/j.lfs.2003.09.047.
12. Dai, C., Tian, E., Hao, Z., Tang, S., Wang, Z., Sharma, G., Jiang, H., and Shen, J. (2022). Aflatoxin B1 Toxicity and Protective Effects of Curcumin: Molecular Mechanisms and Clinical Implications. Antioxidants (Basel, Switzerland), 11(10), 2031. https://doi.org/10.3390/antiox11102031
13. Damiano, S., Jarriyawattanachaikul, W., Girolami, F., Longobardi, C., Nebbia, C., Andretta, E., Lauritano, C., Dabbou, S., Avantaggiato, G., Schiavone, A., Badino., P., and Ciarcia, R. (2022). Curcumin Supplementation Protects Broiler Chickens Against the Renal Oxidative Stress Induced by the Dietary Exposure to Low Levels of Aflatoxin B1. Frontiers of Veterinary Science, 8, 822227. doi: 10.3389/fvets.2021.822227
14. Del Bianchi, M., Oliveira, C.A.F., Albuquerque, R., Guerra, J.L., and Correa, B. (2005). Effects of Prolonged Oral Administration of Aflatoxin B1 and Fumonisin B1 in Broiler Chickens. Poultry Science, 84:1835–1840.
15. Denli, M., Blandon, J.C., Guynot, M.E., Salado, S., and Perez, J.F. (2009). Effects of dietary AflaDetox on performance, serum biochemistry, histopathological changes, and aflatoxin residues in broilers exposed to aflatoxin B1, Poultry Science, 88 (7), 1444-1451. https://doi.org/10.3382/ps.2008-00341.
16. Denli, M., Okan, F., and Doran, F. (2004). Effect of conjugated linoleic acid (CLA) on the performance and serum variables of broiler chickens intoxicated with aflatoxin B1. South African Journal of Animal Science, 34 (2004), 97-103.
17. Godfray, H. C. J., Beddington, J. R., Crute, I. R., Haddad, L., Lawrence, D., Muir, J. F., Pretty, J., Robinson, S., Thomas, S. M., and Toulmin, C. (2010). Food security: The challenge of feeding 9 billion people. Science, 3275(967), 812–818. 10.1126/science.118538
18. Guo, J., Yan, W.R., Tang, J.K., Jin, X., Xue, H.H., Wang, T., Zhang, L.W., Sun, Q.Y., and Liang, Z.X. (2022). Dietary phillygenin supplementation ameliorates aflatoxin B(1)-induced oxidative stress, inflammation, and apoptosis in chicken liver. Ecotoxicology and Environmental Safety, 236:113481. doi: 10.1016/j.ecoenv.2022.113481.
19. Hatab, A. A. , Cavinato, M. E. R. , and Lagerkvist, C. J. (2019). Urbanization, livestock systems and food security in developing countries: A systematic review of the literature. Food Security, 11, 279–299. 10.1007/s12571-019-00906-1
20. Karunaweera, N., Raju, R., Gyengesi, E., and Munch, G. (2015). Plant polyphenols as inhibitors of NF-kappa B induced cytokine production a potential anti-inflammatory treatment for Alzheimer's disease? Frontiers in Molecular Neuroscience, 8:24. doi: 10.3389/fnmol.2015.00024.
21. Khafaga, A.F., and Bayad, A.E. (2016). Impact of Ginkgo biloba extracts on reproductive toxicity induced by single or repeated injection of cisplatin in adult male rats. International Journal Pharmacology, 12: 340-350
22. Kpomasse, C.C., Oke, O.E., Houndonougbo, F.M., and Tona, K. (2021). Broiler production challenges in the tropics: A review. Veterinary Medicine and Science, 7(3), 831–842. https://doi.org/10.1002/vms3.435
23. Li, S., Liu R., Xia, S., Wei, G., Ishfaq, M., Zhang, Y., and Zhang, X. (2022). Protective role of curcumin on aflatoxin B1-induced TLR4/RIPK pathway mediated-necroptosis and inflammation in chicken liver. Ecotoxicology and Environmental Safety, 233, 113319. https://doi: 10.1016/j.ecoenv.2022.113319.
24. Mahato, D.K., Lee, K.E., Kamle, M., Devi, S., Dewangan, K.N., Kumar, P. and Kang, S.G. (2019). Aflatoxins in Food and Feed: An Overview on Prevalence, Detection and Control Strategies. Frontiers in Microbiology, 10, 2266. https://doi: 10.3389/fmicb.2019.02266
25. Marin, D.E. and Taranu, I. (2012). Overview on aflatoxins and oxidative stress. Toxin Reviews, 31(3), 32-43.
26. Medina, A., Gilbert, M. K., Mack, B. M., OBrian, G. R., Rodríguez, A., Bhatnagar, D., Payne, G., and Magan, N. (2017). Interactions between water activity and temperature on the Aspergillus flavus transcriptome and aflatoxin B1 production. International Journal of Food Microbiology, 256, 36–44. https://doi.org/10.1016/j.ijfoodmicro.2017.05.020
27. Mehrzad, J., Devriendt, B., Baert, K., and Cox, E. (2014). Aflatoxin B(1) interferes with the antigen-presenting capacity of porcine dendritic cells. Toxicology in Vitro, 28:531–537.
28. Mousavi Razi, B., Roostaei Ali Mehr, M., and Mohiti Asli, M. (2017). Effect of walnut green husk (Juglans regia) powder on immune responses of broiler chickens. Iranian Veterinary Journal, 13(2), 86-95. doi: 10.22055/ivj.2017.50827.1712
29. Morrison, D.M., Ledoux, D.R., Chester, L.F.B., and Samuels, C.A.N. (2017). A limited survey of aflatoxins in poultry feed and feed ingredients in Guyana. Veterinary Sciences, 4 (4), 60. https://DOI: 10.3390%2Fvetsci4040060.
30. NRC (1994). Nutritent Requirements of Poultry. Ninth Revised Edition. The National Academies Press. Pp. 29. http://nap.edu/2114
31. O’Brien, E., and Dietrich, D.R. (2004). Mycotoxins affecting the kidney. First published in: Toxicology of Kidney. Ed. J.B Hook et al. Boca Raton: CRC Press. Pp. 895-936. http://www.crcpress.com/
32. Oloruntola, O.D., Agbede, J.O., Onibi, G.E., Igbasan, F.A., Ayodele, S.O. Arogunjo, M.A. and Ogunjo, S.T. (2018). Rabbits fed fermented cassava starch residue I: Effect on performance and health status. Archivos de Zootecnia, 67(260), 578-586.
33. Oloruntola, O. D. (2022). Juglans regia kernel meal; A prospective nutraceutical feed supplement. Biotech Studies, 31(2), 87-94. http://doi.org/10.38042/biotechstudies.1222785
34. Pathaw, N., Devi, K. S., Sapam, R., Sanasam, J., Monteshori, S., Phurailatpam, S., Devi, H. C., Chanu, W. T., Wangkhem, B., and Mangang, N. L. (2022). A comparative review on the anti-nutritional factors of herbal tea concoctions and their reduction strategies. Frontiers in Nutrition, 9, 988964. https://doi.org/10.3389/fnut.2022.988964
35. Popescu, R. G., Voicu, S. N., Pircalabioru, G. G., Ciceu, A., Gharbia, S., Hermenean, A., Georgescu, S. E., Panaite, T. D., and Dinischiotu, A. (2020). Effects of Dietary Inclusion of Bilberry and Walnut Leaves Powder on the Digestive Performances and Health of Tetra SL Laying Hens. Animals, 10(5), 823. https://doi.org/10.3390/ani10050823
36. Quezada, T., Cuéllar, H., Jaramillo-Juárez, F., Valdivia, A.G. and Reyes, J.L (2000). Effects of aflatoxin B1 on the liver and kidney of broiler chickens during development, Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 125 (3), 265-272. https://doi.org/10.1016/S0742-8413(99)00107-3.
37. Quezada, T., Cuellar, H., Jaramillo-Juarez, F., Valdivia, A.G. and Reyes, J.L. (2000). Effects of aflatoxin B1 on the liver and kidney of broiler chickens during development. Comparative Biochemistry and Physiology Part C, 125 (2000), 265 – 272.
38. Rosa, C.A., Miazzo, R., Magnoli, C., Salvano, M., Chiac, S.M., Ferrero, S., Saenz, M., Carvalho, E.C. and Dalcero, A. (2001): Evaluation of the efficacy of bentonite from the south of Argentina to ameliorate the toxic effects of aflatoxin in broilers. Poultry Science, 80, 139–144.
39. Safameher, A. (2008). Effects of clinoptilolite on performance, biochemical parameters and hepatic lesions in broiler chickens during aflatoxicosis. Journal of Animal Veterinary Advances, 7, 381-388.
40. Sarma, U.P., Bhetaria, P.J., Devi, P. and Varma, A. (2017). Aflatoxins: implications on health. Indian Journal of Clinical Biochemistry, 32 (2), 124-133. DOI: 10.1007%2Fs12291-017-0649-2.
41. Seifi, S., Sadighara, P. and Mohajer, A. (2022). Protective effects of Aloe vera powder supplementation on some quantitative and qualitative characteristics of egg, histopathological changes and serum biochemistry of laying hens fed by Aflatoxin B1. Veterinary Research Forum, 13 (4) 507 – 512. doi: 10.30466/vrf.2021.530920.3186.
42. Shah, U. N., Mir, J. I., Ahmed, N., Jan, S., and Fazili, K. M. (2018). Bioefficacy potential of different genotypes of walnut Juglans regia L. Journal of food science and technology, 55(2), 605–618. https://doi.org/10.1007/s13197-017-2970-4
43. Sirajudeen, M., Gopi, K., Tyagi, J.S., Moudgal, R.P. Mohan, J. and Singh, R. (2011). Protective effects of melatonin in reduction of oxidative damage and immunosuppression induced by aflatoxin B1-contaminated diets in young chicks. Environmental Toxicology, 26( 2), 153 -160.
44. Sohn, D.H., Kim, Y.C., Oh, S.H., Park, E.J., Li, X. and Lee, B.H. (2003). Hepatoprotective and free radical scavenging effects of Nelumbo nucifera. Phytomedicine 10, 165–169. doi: 10.1078/094471103321659889
45. Taha, N.A. and Al-wadaan, M.A. (2021). Significance and use of walnut, Juglans regia Linn: A review. Advanced Journal of Microbiology Research, 15 (1), 001-010.
46. Tessari, E.N., Kobashigawa, E., Cardoso, A.L., Ledoux, D.R., Rottinghaus, G.E. and Oliveira, C. A. (2010). Effects of aflatoxin B(1) and fumonisin B(1) on blood biochemical parameters in broilers. Toxins, 2(4), 453–460. https://doi.org/10.3390/toxins2040453
47. Tothova, C., Nagy, O. and Kovac, G. (2016). Serum proteins and their diagnostic utility in veterinary medicine: a review. Veterinarni Medicina, 61, 2016 (9), 475–49.
48. Valchev, I., Kanakov, D., Hristov, T. and Lavarov, L. (2014). Investigations on the liver function of broiler chickens with experimental aflatoxicosis. Bulgarian Journal of Veterinary Medicine, 17(4), 302-313.
49. Valchev, I., Kanakov, D., Ts. Hristov, Ts., Lazarov, L., Binev, R., Grozeva, N. and Nikolov, Y. (2014). Effects of experimental aflatoxicosis on renal function in broiler chickens. Bulgarian Journal of Veterinary Medicine, 17(4), 314-324.
50. Verma, J., Swain, B.K. and Johri, T.S. (2002). Effect of various levels of aflatoxin and ochratoxin A and combinations thereof on protein and energy utilisation in broilers. Journal of Science of Food and Agriculture, 82, 1412-1417.
51. Weaver, A.C., See, M.T., Hansen, J.A., Kim, Y.B., De Souza, A.L. and Middleton, T.F. (2013). The use of feed additives to reduce the effects of aflatoxin and deoxynivalenol on pig growth, organ health and immune status during chronic exposure. Toxins (Basel), 5, 1261–1281.
52. Xu, D.P., Li, Y., Meng, X., Zhou, T., Zhou, Y., Zheng, J., Zhang, J.J. and Li, H.B. (2017). Natural Antioxidants in Foods and Medicinal Plants: Extraction, Assessment and Resources. International Journal of Molecular Sciences, 18(1), 96. https://doi.org/10.3390/ijms18010096
53. Yamashita, Y., Ueyama, T., Nishi, T., Yamamoto, Y., Kawakoshi, A., Sunami, S., Iguchi, M., Tamai, H., Ueda, K., Ito, T., Tsuruo, Y. and Ichinose, M. (2014). Nrf2-inducing anti-oxidation stress response in the rat liver--new beneficial effect of lansoprazole. PloS one, 9(5), e97419. https://doi.org/10.1371/journal.pone.0097419
54. Zhao, F., Ci, X, Man, X., Li, J., Wei, Z. and Zhang, S. (2021). Food-Derived Pharmacological Modulators of the Nrf2/ARE Pathway: Their Role in the Treatment of Diseases. Molecules, 26(4):1016. doi: 10.3390/molecules26041016.