Juglans kernel powder and jacobinia leaf powder supplementation influenced growth, meat, brain, immune system and dna biomarker of broiler chickens fed Aflatoxin-B1 contaminated diets

Year 2024, , 33 - 42, 30.06.2024

Olugbenga David Oloruntola

https://doi.org/10.38042/biotechstudies.1442037

Abstract

This study investigates the impact of Juglans kernel powder (JKP) and Jacobinia leaf powder (JLP) supplementation on Aflatoxin-B1 (AF) exposed broiler chickens. 200 Cobb-500 broiler chicks were grouped to four treatment: CONT: No supplement; AFNS: 0.5 mg/kg AF; AFJK: 0.5 mg/kg AF+ 350 mg/kg JKP; AFJL: 0.5 mg/kg AF+350 mg/kg JLP. On day 42, the broiler chicken’s relative growth rate, and dressed percentage were lowest in AFNS compared to the rest treatments. Meat cholesterol was lower in AFNS, AFJK, and AFJL, compared to CONT. Meat catalase in AFNS was lower than those in CONT, AFJK, and AFJL. Meat glutathione peroxidase levels of birds in AFNS are similar to AFJL but were lower than those in CONT, and AFJK. Lipid oxidation, and protein oxidation activities of broiler chickens in AFNS were higher than those in the rest of the treatments. Brain catalase, acetylcholinesterase, and glutathione peroxidase activities of birds in AFNS were lower than CONT, AFJK, and AFJL. Expressions of proinflammatory cytokines, and 8-hydroxy-2'-deoxyguanosine in AFNS were higher compared to other treatments. The immunoglobulins A, E and G of broiler chickens in AFNS were lower than CONT, AFJK, and AFJL. 350 mg/kg JKP or JLP ameliorate the effects of AF contamination on broiler chickens.

Keywords

Antioxidants, Immune response, Phytosupplement, Mycotoxins, Poultry

Ethical Statement

The animal care and use procedure was approved by the Animal Care and Use Committee of the Department of Animal Science at Adekunle Ajasin University in Akungba Akoko, Nigeria.

References

• Abbas, Z. K., Saggu, S., Sakeran, M. I., Zidan, N., Rehman, H., & Ansari, A. A. (2015). Phytochemical, antioxidant and mineral composition of hydroalcoholic extract of chicory (Cichorium intybus L.) leaves. Saudi Journal of Biological Sciences, 22(3), 322–326. https://doi.org/10.1016/j.sjbs.2014.11.015
• Adebayo, F. B., Adu, O. A., Chineke, C. A., Oloruntola, O. D., Omoleye, O. S., Adeyeye, S. A., & 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 Sciences, 6(4), 54-61.
• Allam, G., Abuelsaad, A. S. A., Alblihed, M. A., & Alsulaimani, A. A. (2016). Ellagic acid reduces murine Schistosomiasis mansoni immunopathology via up-regulation of IL-10 and down-modulation of pro-inflammatory cytokines production. Immunopharmacology and Immunotoxicology, 38(4), 286-297. https://doi.org/10.1080/08923973.2016.1189561
• An, Y., Shi, X., Tang, X., Wang, Y., Shen, F., Zhang, Q., Wang, C., Jiang, M., Liu, M., & Yu, L. (2017). Aflatoxin B1 Induces Reactive Oxygen Species-Mediated Autophagy and Extracellular Trap Formation in Macrophages. Frontiers in Cellular and Infection Microbiology, 7, 53. https://doi.org/10.3389/fcimb.2017.00053
• AOAC. (2010). Official method of analysis, 18th edition. Association of Official Analytical Chemists, Washington D.C.
• Ayodele, S. O., Oloruntola, O. D., & Agbede, J. O. (2016). Effect of diet containing Alchornea cordifolia leaf meal and enzyme supplementation on performance and digestibility of Weaner rabbits. World Rabbit Science, 24, 201-206. https://doi.org/10.4995/wrs.2016.3933
• Azqueta, A., & Collins, A. (2016). Polyphenols and DNA Damage: A Mixed Blessing. Nutrients, 8(12), 785. https://dx.doi.org/10.3390/nu8120785
• Benzie, I. F., & Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": The FRAP assay. Analytical Biochemistry, 239(1), 70-6. https://doi.org/10.1006/abio.1996.0292
• Brown, R., Priest, E., Naglik, J. R., & Richardson, J. P. (2021). Fungal Toxins and Host Immune Responses. Frontier Microbiology, 12, 643639. https://doi.org/10.3389/fmicb.2021.643639
• Burel, S. D., Favrot, M. C., Fremy, J. M., Massimi, C., Prigent, P., Debongnie, L. P., & 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. https://doi.org/10.2903/sp.efsa.2009.EN-22
• Cichoski, A.J., Rotta, R.B., Scheuermann, G., Junior, A.C., & Barin, J.S. (2012). Investigation of glutathione peroxidase activity in chicken meat under different experimental conditions. Food Science and Technology, 32(4), 661-667. https://doi.org/10.1590/S0101-20612012005000107
• Cortinas, L., Barroeta, A., Villaverde, C., Galobart, J., Guardiola, F., & Baucells, D. (2005). Influence of the dietary polyunsaturation level on chicken meat quality: Lipid oxidation. Poultry Science, 84, 48-55. https://doi.org/10.1093/ps/84.1.48
• Da Silva, E. O., Bracarense, A. P. F. L., & Oswald, I. P. (2018). Mycotoxins and oxidative stress: Where are we? World Mycotoxin Journal, 11, 113–134. https://doi.org/10.3920/WMJ2017.2267
• De Ruyck, K., De Boevre, M., Huybrechts, I., & De Saeger, S. (2015). Dietary mycotoxins, co-exposure, and carcinogenesis in humans: Short review. Mutation Research. Review in Mutatation Research, 766, 32–41. https://doi.org/10.1016/j.mrrev.2015.07.003
• El-Haleem, A., Reda, M., & Mohamed, D. A. (2011). The effects of experimental aflatoxicosis on the pancreas of adult male albino rats and the role of ginger supplementation a histological and biochemical study. The Egyptian Journal of Histology, 34(3), 423-435. https://doi.org/10.1097/EHX.0000398847.67845.55
• Feng, W. H., Xue, K. S., Tang, L., Williams, P. L., & Wang, J. S. (2016). Aflatoxin B₁-Induced Developmental and DNA Damage in Caenorhabditis elegans. Toxins, 9(1), 9. https://doi.org/10.3390/toxins9010009.
• Forni, C., Facchiano, F., Bartoli, M., Pieretti, S., Facchiano, A., D'Arcangelo, D., Norelli, S., Valle, G., Nisini, R., Beninati, S., Tabolacci, C., & Jadeja, R. N. (2019). Beneficial Role of Phytochemicals on Oxidative Stress and Age-Related Diseases. BioMed Research International, 2019, 8748253. https://doi.org/10.1155/2019/8748253
• Fouad, A. M., Ruan, D., El-Senousey, H. K., Chen, W., Jiang, S., & Zheng, C. (2019). Harmful Effects and Control Strategies of Aflatoxin B₁ Produced by Aspergillus flavus and Aspergillus parasiticus Strains on Poultry: Review. Toxins, 11(3), 176. https://doi.org/10.3390/toxins11030176
• Freitas, A. P., Santos, C. R., Sarcinelli, P. N., Silva Filho, M. V., Hauser-Davis, R. A., & Lopes, R. M. (2016). Evaluation of a Brain Acetylcholinesterase Extraction Method and Kinetic Constants after Methyl-Paraoxon Inhibition in Three Brazilian Fish Species. PloS One, 11(9), e0163317. https://doi.org/10.1371/journal.pone.0163317
• Gautam, R., & Jachak, S. M. (2009). Recent developments in anti-inflammatory natural products. Medicinal Research Reviews, 29(5), 767–820. 10.1002/med.20156.
• Guengerich, F. P., Johnson, W. W., Shimada, T., Ueng, Y. F., Yamazaki, H., & Langouet, S. (1998). Activation and detoxication of Aflatoxin B1. Mutatation Research, 402:121–128. https://doi/10.1016/S0027-5107(97)00289-3
• Gugliandolo, E., Peritore, A. F., D'Amico, R., Licata, P., & Crupi, R. (2020). Evaluation of Neuroprotective Effects of Quercetin against Aflatoxin B1-Intoxicated Mice. Animals: An Open Access Journal from MDPI, 10(5), 898. https://doi.org/10.3390/ani10050898
• Guo, C., Li, X., Wang, R., Yu J., Ye, M., Mao, L., Zhang, S., & Zheng, S. (2016). Association between Oxidative DNADamage and Risk of Colorectal Cancer: Sensitive Determination of Urinary 8-Hydroxy-2′-deoxyguanosine by UPLC-MS/MS Analysis. Scientific Reports, 6, 32581 (2016). https://doi.org/10.1038/srep32581
• Hashemi, S. R., & Davoodi, H. (2010). Phytogenics as new class of feed additive in poultry industry. Journal of Animal and Veterinary Advances, 9, 2295–2304.
• Houndonougbo, M. F., Chwalibog, A., & Chrysostome, C. A. A. M. (2012). Effect of processing on feed quality and bio‐economic performances of broiler chickens in Benin. International Journal of Applied Poultry Research, 1(2), 47–54.
• Huang, B., Chen, Q., Wang, L., Gao, X., Zhu, W., Mu, P., & Deng, Y. (2020). Aflatoxin B1 Induces Neurotoxicity through Reactive Oxygen Species Generation, DNA Damage, Apoptosis, and S-Phase Cell Cycle Arrest. International Journal of Molecular Sciences, 21(18), 6517. https://doi.org/10.3390/ijms21186517
• Juan, C., Ritieni, A., and Mañes, J. (2012). Determination of trichothecenes and zearalenones in grain cereal, flour and bread by liquid chromatography tandem mass spectrometry. Food Chemistry, 134, 2389–2397. https://doi.org/10.1016/j.foodchem.2012.04.051
• Keppler, J. K., Schwarz, K., & van der Goot, A. J. (2020). Covalent modification of food proteins by plant-based ingredients (polyphenols and organosulphur compounds): A commonplace reaction with novel utilization potential. Trends in Food Science and Technology, 101 (2020), 38-49. https://doi.org/10.1016/j.tifs.2020.04.023
• Khan, R. A., Khan, M. R., & Sahreen, S. (2012). Brain antioxidant markers, cognitive performance and acetylcholinesterase activity of rats: efficiency of Sonchus asper. Behavioral and Brain Functions, 8, 21. https://doi.org/10.1186/1744-9081-8-21
• Kpomasse, C. C., Oke, O. E., Houndonougbo, F. M., & 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
• Kraft, S., Buchenauer, L., & Polte, T. (2021). Mold, Mycotoxins and a Dysregulated Immune System: A Combination of Concern. International Journal of Molecular Sciences, 22(22), 12269. https://doi.org/10.3390/ijms222212269
• Kumar, G. P., & Khanum, F. (2012). Neuroprotective potential of phytochemicals. Pharmacognosy Reviews, 6(12), 81–90. https://doi.org/10.4103/0973-7847.99898
• Lee, M. T., Lin, W. C., Yu, B., & Lee, T. T. (2017). Antioxidant capacity of phytochemicals and their potential effects on oxidative status in animals - A review. Asian-Australasian Journal of Animal Sciences, 30(3), 299–308. https://doi.org/10.5713/ajas.16.0438
• Li, H., Guan, K., Zuo, Z., Wang, F., Peng, X., Fang, J., Cui, H., Zhou, Y., Ouyang, P., Su, G., & Chen, Z. (2019). Effects of aflatoxin B1 on the cell cycle distribution of splenocytes in chickens. Journal of Toxicologic Pathology, 32(1), 27–36. https://doi.org/10.1293/tox.2018-0015
• Mahato, D. K., Lee, K. E., Kamle, M., Devi, S., Dewangan, K. N., Kumar, P., & Kang, S.G. (2019). Aflatoxins in Food and Feed: An Overview on Prevalence, Detection and Control Strategies. Frontier in Microbiology, 10, 2266. https://doi.org/10.3389/fmicb.2019.02266
• Maheshwari, S., Kumar, V., Bhadauria, G., & Mishra, A. (2022). Immunomodulatory potential of phytochemicals and other bioactive compounds of fruits: A review. Food Frontiers. 3 (2), 221-238. https://doi.org/10.1002/fft2.129
• Mahoney, N., & Molyneux, R. J. (2004). Phytochemical Inhibition of Aflatoxigenicity in Aspergillus flavus by Constituents of Walnut (Juglans regia). Journal of Agricultural and Food Chemistry, 52 (7), 1882–1889. https://doi.org/10.1021/jf030812p
• Min, B., Nam, K. C., Cordray, J., & Ahn, D. U. (2008). Endogenous factors affecting oxidative stability of beef loin, pork loin, and chicken breast and thigh meats. Journal of Food Science, 73, 439–446. https://doi.org/10.1111/j.1750-3841.2008.00805.x
• Mohammed, A. M. & Metwally, N. S. (2009). Antiaflatoxicogenic activities of some aqeous plant extracts against AFB1 induced Renal and Cardiac damage. Journal of Pharmacology and Toxicology, 4 (1), 1-16. https://doi.org/10.3923/jpt.2009.1.16
• Muhlisin, M., Utama, D.T., Lee, J.H., Choi, J.H., & Lee, S.K. (2016). Antioxidant enzyme activity, iron content and lipid oxidation of raw cooked meat of Korean native chickens and other poultry. Asian-Australasian Journal of Animal Sciences, 29(5), 695–701. https://doi.org/10.5713/ajas.15.0256
• Nazarizadeh, H., Mohammad Hosseini, S., & Pourreza, J. (2019). ‘Effect of plant extracts derived from thyme and chamomile on the growth performance, gut morphology and immune system of broilers fed aflatoxin B1 and ochratoxin A contaminated diets’, Italian Journal of Animal Science, 18, 1073-1081. https://doi.org/10.1080/1828051X.2019.1615851
• Nordberg, J., & Arnér, E. S. J. (2001). Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radical Biology and Medicine, 31(11), 1287–1312. https://doi.org/10.1016/S0891-5849(01)00724-9
• Olarotimi, O. J., Gbore, F. A., Adu, O. A., Oloruntola, O. D., & Falowo, A. B. (2022). Effects of ginger meal supplementation on performance and meat antioxidative enzymes of broilers fed monosodium glutamate. Acta Fytotechn Zootechn, 25, 2022(3), 174–184. https://doi.org/10.15414/afz.2022.25.03.174-184
• Oloruntola, O. D. (2022a). Juglans regia kernel meal; A prospective nutraceutical feed supplement. Biotech Studies, 31(2), 87-94. https://doi.org/10.38042/biotechstudies.1222785
• Oloruntola, O. D. (2022b). Utilization of processed kola nut husk meal in poultry: Effects on the performance, carcass, biochemical indicators and antioxidant enzymes of broiler chickens. Waste and Biomass Valorization, 13(3). https://doi.org/10.1007/s12649-022-01730-z
• Oloruntola, O. D., Ayodele, S. O., Adeyeye, S. A., Fasuhami, O. S., Osowe C. O., & Ganiyu, T. O. (2022a). Proximate composition, phytochemical profile, antioxidant, antidiabetic and anti-inflammatory properties of Justicia carnea leaf powder. Black Sea Journal of Agriculture, 5(4), 415-423. https://doi.org/10.47115/bsagriculture.1145262
• Oloruntola, O. D., Ayodele, S. O., Agbede, J. O., Oloruntola, D..A., Ogunsipe, M. H., & Omoniyi, I. S. (2016). Effect of Alchornea cordifolia leaf meal and enzyme supplementation on growth, haematological, immunostimulatory and serum biochemical response of rabbits. Asian Journal of Biological and Life Sciences, 5(2), 190-195.
• Oloruntola, O. D., Ayodele, S. O., Omoniyi, I. S., Adeyeye, S. A., & Adegbeye, M. J. (2022b). The effect of dietary supplementation of Mucuna leaf meal on the growth performance, blood parameters, and carcass quality of broilers. Acta Scientiarum, V44, e55362. https://doi.org/10.4025/actascianimsci.v44i1.55362
• Oloruntola, O. D., Agbede, J. O., Onibi, G. E., Igbasan, F. A., Ayodele, S. O. Arogunjo, M. A & Ogunjo, S. T (2018). Rabbits fed fermented cassava starch residue I: Effect on performance and health status. Archivos de Zootecnia, 67(260), 578-586.
• Osowe, C. O., Adu, O. A., Oloruntola, O. D., Chineke, C. A., Atansuyi, A. J. & Olateju, I. S. (2022). The impact of breed, Ficus exasperata leaf powder and vitamin C on carcass traits, brain and meat oxidative enzymes of broiler chickens raised under the tropical condition. Tropical Animal Health and Production, 54(6), 404. https://doi.org/10.1007/s11250-022-03386-2
• Pankaj, S. K., Shi, H., & Keener, K. M. (2018). A review of novel physical and chemical decontamination technologies for aflatoxin in food. Trends Food Science and Technology, 71, 73–83. https://doi.org/10.1016/j.tifs.2017.11.007
• Perez-Gregorio, R., & Simal-Gandara, J. (2017). A critical review of bioactive food components, and of their functional mechanisms, biological effects and health outcomes. Current Pharmaceutical Design, 23(19), 2731–41. https://doi.org/10.2174/1381612823666170317122913
• Pitt, J. I., & Miller, J. D. (2017). A concise history of mycotoxin research. Journal of Agriculture and Food Chemistry, 65, 7021–7033. https://doi.org/10.1021/acs.jafc.6b04494
• Ponte, P. I. P., Mendes, I., Quaresma, M., Aguiar, M. N. M., Lemos, J. P. C., Ferreira, L. M. A., Soares, M. A. C., Alfaia, C. M., Prates, J. A. M., & Fontes, C. M. G. A. (2004). Cholesterol Levels and Sensory Characteristics of Meat from Broilers Consuming Moderate to High Levels of Alfalfa. Poultry Science, 83, 810–814. https://doi.org/10.1093/ps/83.5.810
• Pueyo, I. U., & Calvo, M. I. (2009). Phytochemical Study and Evaluation of Antioxidant, Neuroprotective and Acetylcholinesterase Inhibitor Activities of Galeopsis ladanum L. extracts. Pharmacognosy Magazine, 5, 287–290. https://dx.doi.org/10.4103/0973-1296.58146
• Sadeghi, A., Ghahari, L., & Yousefpour, M. (2019). Vitamin E Supplementation Reduces Oxidative Stress in the Male Wistar Rats’ Brain Against Polyvinyl Chloride Products. Annals of Military and Health Sciences Research, 17(2):e92768. https://doi.org/10.5812/amh.92768
• Saleh, H. A., Yousef, M. H., & Abdelnaser, A. (2021). The Anti-Inflammatory Properties of Phytochemicals and Their Effects on Epigenetic Mechanisms Involved in TLR4/NF-κB-Mediated Inflammation. Frontiers in Immunology, 12, 606069. https://doi.org/10.3389/fimmu.2021.606069
• Sarma, U. P., Bhetaria, P. J., Devi, P., & Varma, A. (2017). Aflatoxins: Implications on Health. Indian Journal of Clinical Biochemistry, 32(2), 124–133. https://doi.org/10.1007/s12291-017-0649-2
• Silva, Filho, M. V., Oliveira, M. M., Salles, J. B., Bastos, V. L., Cassano, V. P., & Bastos, J. C. (2004). Methyl-paraoxon comparative inhibition kinetics for acetylcholinesterases from brain of neotropical fishes. Toxicology Letters, 153(2), 247–254. https://doi.org/10.1016/j.toxlet.2004.04.026
• Smet, K., Raes, K., Huyghebaert, G., Haak, L., Arnouts, S., & De Smet, S. (2008). Lipid and Protein Oxidation of Broiler Meat as Influenced by Dietary Natural Antioxidant Supplementation, Poultry Science, 87 (8), 1682-1688. https://doi.org/10.3382/ps.2007-00384
• Soltani, D. M., Shahryar H.A., Hosseini, S. A., Ebrahimnezhad, Y., & Aghashahi, A. (2019). Effects of dietary inclusion of commercial toxin binders and prebiotics on performance and immune responses of broiler chicks fed aflatoxin-contaminated diets. South African Journal of Animal Science, 49(2), 322-331. https://dx.doi.org/10.4314/sajas.v49i2.12
• Souza, M. A. A., Visentainer, J. V., Carcalho, R. H., Garcia, F., Ida, E. I & Shimokomaki, M. (2013). Lipid and protein oxidation in charqui meat and jerked beef. Brazilian Archives of Biology and Technology, 56(1), 107-112. https://doi.org/10.1590/S1516-89132013000100014
• Sur, E. & Celik, I. (2003). Effect of aflatoxin B1 on the development of the bursa of Fabricius and blood lymphocyte acid phosphatase of the chicken. British Poultry Science, 44, 558-566. https://doi.org/10.1080/00071660310001618352
• Tallentire, C. W., Leinonen, I., & Kyriazakis, I. (2016). Breeding for efficiency in the broiler chicken: A review. Agronomy for Sustainable Development, 36, 66. https://doi.org/10.1007/s13593-016-0398-2
• Thinh, N. H., Vinh, N. T., Linh, N. V., Giang, N. T. P., Doan, B. H., & Dang, P. K. (2018). Effect of dietary supplementation with green tea powder on performance characteristic, meat organoleptic quality and cholesterol content of broilers. Livestock Research for Rural Development, 30(9). http://www.lrrd.org/lrrd30/9/nhti30160.html
• Tokur, B., Korkmaz, K., & Ayas, D. (2006). Comparison of two Thiobarbituric Acid (TBA) Method for monitoring lipid oxidation in fish. EU Journal of Fisheries and Aquatic Science, 23(3 4), 331–334.
• Towner, R. A., Qian, S. Y., Kadiiska, M. B., & Mason, R. P. (2003). In vivo identification of aflatoxin-induced free radicals in rat bile. Free Radical Biology and Medicine, 35, 1330–1340. https://doi.org/10.1016/j.freeradbiomed.2003.08.002
• Udomkun, P., Wiredu, A. N., Nagle, M., Müller, J., Vanlauwe, B., & Bandyopadhyay, R. (2017). Innovative technologies to manage aflatoxins in foods and feeds and the profitability of application–A review. Food Control, 76, 127–138. https://doi.org/10.1016/j.foodcont.2017.01.008
• Uijttenboogaart, T.G., (1999). European perspective on poultry slaughter technology. Poultry Science, 78, 295-297. https://doi.org/10.1093/ps/78.2.295
• Valavanidis, A., Vlachogianni, T., & Fiotakis, C. (2009). 8-hydroxy-2' -deoxyguanosine (8-OHdG): A critical biomarker of oxidative stress and carcinogenesis. Journal of environmental science and health. Part C. Environmental Carcinogenesis and Ecotoxicology Reviews, 27(2), 120–139. https://doi.org/10.1080/10590500902885684
• Valenzuela-Grijalva, N. V., Pinelli-Saavedra, A., Muhlia-Almazan, A., Domínguez-Díaz, D., & González-Ríos, H. (2017). Dietary inclusion effects of phytochemicals as growth promoters in animal production. Journal of Animal Science and Technology, 59, 8. https://doi.org/10.1186/s40781-017-0133-9
• Ye, Y., Ma, Y., Kong, M., Wang, Z., Sun, K., & Li, F. (2023). Effects of Dietary Phytochemicals on DNA Damage in Cancer Cells. Nutrition and Cancer, 75(3), 761–775. https://doi.org/10.1080/01635581.2022.2157024
• Zhang, C., Nestorova, G., Rissman R. A., & Feng, J. (2013).Detection and quantification of 8-hydroxy-2'-deoxyguanosine in Alzheimer's transgenic mouse urine using capillary electrophoresis. Electrophoresis, 34(15), 2268-74. https://doi.org/10.1002/elps.201300036
• Zhen, Y., & Zhang H. (2019). NLRP3 Inflammasome and Inflammatory Bowel Disease. Frontiers in Immunology, 10, 276. https://doi.org/10.3389/fimmu.2019.00276