| More

Immunological and pathological adverse effects of avian influenza virus subtype H9N2 infection in aflatoxicated-broiler chickens

Views: 526 Downloads: 178
H.F. ELLAKANY, H.S. ABD-ELHAMID, L.A. TANTAWY, H.A. ELSAMADONY, A.R. ELBESTAWY, A.R. GADO, Y.S. EL-SAYED, H.S. ISMAEL
H.F. ELLAKANY, H.S. ABD-ELHAMID, L.A. TANTAWY, H.A. ELSAMADONY, A.R. ELBESTAWY, A.R. GADO, Y.S. EL-SAYED, H.S. ISMAEL

Abstract


Aflatoxin B1 (AFB1) is a metabolic product of the Aspergillus spp. of molds, which grow on several feedstuffs stored in hot moist conditions. It is one of the immunosuppressive agents that might influence the pathogenesisof avian influenza virus (AIV) subtype H9N2 in broilers, which can exacerbate the disease outcomes. The immunological, biochemical and pathological adverse health effects of an interaction between low levels of dietary aflatoxins (AFs) and H9N2 infection in broiler chickens were investigated. One hundred and eighty of unvaccinated 1-day-old COBB chicks were, therefore, raised for 35 days in the following treatment groups: control, AFs, AFs+H9N2, and H9N2. AFs in the basal diet was added at 200 ppb starting from the first day of age, while H9N2 virus was intra-nasally installed at a dose of 100 μl of 106 EID50/bird of allantois fluid at 23rd day. Humoral and cell-mediated immune responses were evaluated. Evidence of H9N2-AIV viral shedding was also detected. It has been observed that concurrent exposure of AFs and H9N2 virus negatively affected chicken performance traits i.e. lowered feed intake and body weights with exaggerated respiratory and digestive disturbances, and 20% mortality rate. Ten days’ post H9N2 infection, significant (p≤ 0.05) increment in serum transaminases (AST and ALT) and falling in cell-mediated immunity i.e. total leukocyte count, lymphocyte transformation activity and macrophage phagocytic activity were detected. Additionally, AFs+H9N2 significantly (p≤ 0.05) lowered H9N2-HI titers (5.5 Log2) than H9N2 alone (6.3 Log2). Pathologically, aflatoxicated chickens showed hydropic degeneration, hepatocytic vacuolation and necrosis of liver tissues with nephrosis and urates deposition in ureters, as well as bursal and thymic lesions, which were potent in H9N2–inoculated chickens. AFs exposure increased the incidence and titer of H9N2 viral shedding. It could be concluded that dietary contamination with AFs even at very low levels has explanatory effect in H9N2–inoculated broilers, and vice versa.

Keywords


Aflatoxins; AIV subtype H9N2; Immunological; Pathological; Broilers

Full Text:

PDF

References


Abd El-Hamid H, Ellakany H, Elbestawy A, Gado A (2018) Molecular Characterization of H9N2 Avian Influenza Viruses Isolated from Commercial Broiler Chickens in Egypt during 2014-2015 Alexandria Journal of Veterinary Sciences 56:54 doi:10.5455/ajvs.220473.

Abdel-Wahhab MA, Nada SA, Khalil FA (2002) Physiological and toxicological responses in rats fed aflatoxin-contaminated diet with or without sorbent materials Animal Feed Science and Technology 97:209-219 doi:10.1016/s0377-8401(01)00342-x

Aderem A, Underhill DM (1999) Mechanisms of Phagocytosis in Macrophages Annual Review of Immunology 17:593-623 doi:10.1146/annurev.immunol.17.1.593.

Afzal M, Zahid S (2004) Effects of Addition of a Mycotoxin Detoxifier in Poultry Feed Containing Different Levels of Aflatoxins on the Performance of Broilers Asian Austral J Anim 17:990-994 doi:10.5713/ajas.2004.990.

Ahad A et al. (2013) Serosurveillance to H9 and H7 Avian Influenza Virus among Poultry Workers in Punjab Province, Pakistan Pakistan Veterinary Journal 33:107-112.

Alexander DJ (2003) Report on Avian Influenza in the Eastern Hemisphere During 1997–2002 Avian Dis 47:792-797 doi:10.1637/0005-2086-47.s3.792.

Azizpour A, Moghadam N (2015) Assessment of serum biochemical parameters and pathological changes in broilers with chronic aflatoxicosis fed glucomannan-containing yeast product (Mycosorb) and sodium bentonite Bulletin of the Veterinary Institute in Pulawy 59 doi:10.1515/bvip-2015-0031.

Bakshi CS, Asikdar T, Johri S, Malik M, Singh R (2000) Effect of grade dietary levels of aflatoxin on humoral immune response in commercial broilers Indian Journal of Comparative Microbiology, Immunology, and Infectious Diseases 21 163-164.

Bancroft JD, Gamble M (2002) Theory and Practice of Histological Techniques. 5th edn. Churchill Livingstone, Edinburgh ; New York.

Bano S, Naeem K, Malik SA (2003) Evaluation of pathogenic potential of avian influenza virus serotype H9N2 in chickens Avian Dis 47:817-822 doi:10.1637/0005-2086-47.s3.817.

Basmacioglu H, Oguz H, Ergul M, Col R, Birdane YO (2005) Effect of dietary esterified glucomannan on performance, serum biochemistry and haematology in broilers exposed to aflatoxin Czech Journal of Animal Science 50:31-39.

Celik I, Oguz H, Demet O, Donmez HH, Boydak M, Sur E (2000) Efficacy of polyvinylpolypyrrolidone in reducing the immunotoxicity of aflatoxin in growing broilers British poultry science 41:430-439. doi:10.1080/713654954.

Chen K et al. (2014) Effects of dietary selenium on histopathological changes and T cells of spleen in broilers exposed to aflatoxin B1 International journal of environmental research and public health 11:1904-1913 doi:10.3390/ijerph110201904.

Cusumano V et al. (1996) Immunobiological activities of mould products: functional impairment of human monocytes exposed to aflatoxin B1 Research in Microbiology 147:385-391 doi:10.1016/0923-2508(96)84713-9.

Diener UL, Cole RJ, Sanders TH, Payne GA, Lee LS, Klich MA (1987) Epidemiology of aflatoxin formation by Aspergillus flavus Annual Review of Phytopathology 25:249-270 doi:10.1146/annurev. py.25.090187.001341.

El Miniawy HMF, Ahmed KA, El-Sanousi AA, Khattab MSM (2014) Effect of Aflatoxin Induced Immunosuppression on Pathogenesis of H9N2 Avian Influenza Virus Pakistan Veterinary Journal 34 234-238.

El Miniawy HMF, El-Sanousi AAG, Ahmed KAA, Khattab MMSE (2011) Pathogenesis of low pathogenic strain of avian influenza virus H9N2 in chickens fed on diet containing aflatoxins Toxicology Letters 205:S147 doi:10.1016/j.toxlet.2011.05.520.

Ellakany HF, Abuakkada SS, Oda SS, El-Sayed YS (2011) Influence of low levels of dietary aflatoxins on Eimeria tenella infections in broilers Trop Anim Health Prod 43:249-257 doi:10.1007/s11250-010-9685-0.

Gabal MA, Azzam AH (1998) Interaction of aflatoxin in the feed and immunization against selected infectious diseases in poultry. II. Effect on one-day-old layer chicks simultaneously vaccinated against Newcastle disease, infectious bronchitis and infectious bursal disease Avian Pathol 27:290-295 doi:10.1080/03079459808419338.

Gharaibeh S (2008) Pathogenicity of an avian influenza virus serotype H9N2 in chickens Avian Dis 52:106-110 doi:10.1637/8108-090907-Reg.

Giambrone JJ, Diener UL, Davis ND, Panangala VS, Hoerr FJ (1985) Effects of purified aflatoxin on broiler chickens Poult Sci 64:852-858. doi:10.3382/ps.0640852.

Hablolvarid MH, Sohraby Haghdost I, Pourbakhsh SA, Gholami MR (2004) Histopathological Study of Intratracheally Inoculated A/Chicken/Iran/259/1998 (H9N2) Influenza Virus in Chicken Archives of Razi Institute 58:51-62.

Hadipour MM, Farjadian SH, Azad F, Sheibani N, Olyaie A (2011) Histologic Lesions of Thymus and Bursa of Fabricius in Commercial Broiler Chickens Inoculated with H9N2 Avian Influenza Virus International Journal of Animal and Veterinary Advances 3:186-188.

Hatori Y, Sharma RP, Warren RP (1991) Resistance of C57B1/6 mice to immunosuppressive effects of aflatoxin B1 and relationship with neuroendocrine mechanisms Immunopharmacology 22:127-136. doi:10.1016/0162-3109(91)90037-y.

He Y et al. (2014) Effects of sodium selenite on aflatoxin B1-induced decrease of ileal IgA+ cell numbers and immunoglobulin contents in broilers Biological trace element research 160:49-55 doi:10.1007/s12011-014-0035-3.

Hs A, Hf E, Ha H, Ar E, Km A (2016) Pathogenicity of an Avian Influenza H9N2 Virus isolated From Broiler Chickens in Egypt Alexandria Journal of Veterinary Sciences 51:90 doi:10.5455/ajvs.236275.

Hu P et al. (2018) The molecular mechanism of cell cycle arrest in the Bursa of Fabricius in chick exposed to Aflatoxin B 1 Sci Rep 8:1770. doi:10.1038/s41598-018-20164-z.

Iheshiulor OOM, Esonu BO, Chuwuka OK, Omede AA, Okoli IC, Ogbuewu IP (2011) Effects of mycotoxins in animal nutrition: A review Asian Journal of Animal Sciences 5:19-33 doi:10.3923/ajas.2011.19.33.

Jain NC (2000) Schalm’s Veterinary Haematology. 5th edn. Lea and Fabiger, Philadelphia.

Jiang M, Peng X, Fang J, Cui H, Yu Z, Chen Z (2015) Effects of aflatoxin b1 on T-cell subsets and mRNA expression of cytokines in the intestine of broilers Int J Mol Sci 16:6945-6959 doi:10.3390/ijms16046945.

Kishida N, Sakoda Y, Eto M, Sunaga Y, Kida H (2004) Co-infection of Staphylococcus aureus or Haemophilus paragallinarum exacerbates H9N2 influenza A virus infection in chickens Arch Virol 149:2095-2104 doi:10.1007/s00705-004-0372-1.

Kubena LF, Harvey RB, Huff WE, Corrier DE, Phillips TD, Rottinghaus GE (1990) Efficacy of a hydrated sodium calcium aluminosilicate to reduce the toxicity of aflatoxin and T-2 toxin Poult Sci 69:1078-1086.

Kumar PA, Das SK (1996) A colorimetric assay to evaluate the cytotoxic activity of the intestinal intraepithelial lymphocytes of chickens Vet Res Commun 20:513-518.

Kwon JS et al. (2008) Immune responses and pathogenesis in immunocompromised

chickens in response to infection with the H9N2 low pathogenic avian influenza virus Virus Res 133:187-194. doi:10.1016/j.virusres.2007.12.019.

Liu T, Ma Q, Zhao L, Jia R, Zhang J, Ji C, Wang X (2016) Protective Effects of Sporoderm-Broken Spores of Ganderma lucidum on Growth Performance, Antioxidant Capacity and Immune Function of Broiler Chickens Exposed to Low Level of Aflatoxin B(1) Toxins (Basel) 8:278 doi:10.3390/toxins8100278.

Marchioro A et al. (2013) Effects of Aflatoxins on Performance and Exocrine Pancreas of Broiler Chickens Avian Dis 57:280-284. doi:10.1637/10426-101712-Reg.1.

Mohaghegh A, Chamani M, Shivazad M, Sadeghi AA, Afzali N (2016) Effect of esterified glucomannan on broilers exposed to natural mycotoxin-contaminated diets J Appl Anim Res 45:285-291 doi:10.108. 0/09712119.2016.1174122.

Nabney J, Nesbitt BF (1965) A spectrophotometric method for determining the aflatoxins The Analyst 90:155 doi:10.1039/an9659000155.

Neldon-Ortiz DL, Qureshi MA (1991) Direct and microsomal activated aflatoxin B1 exposure and its effects on turkey peritoneal macrophage functions in vitro Toxicology and applied pharmacology 109:432-442.

Oguz H, KeÇEci T, Birdane YO, ÖNder F, Kurtoglu V (2000) Effect of clinoptilolite on serum biochemical and haematological characters of broiler chickens during aflatoxicosis Research in Veterinary Science 69:89-93 doi:10.1053/rvsc.2000.0395.

Ortatatli M, Oguz H, Hatipoglu F, Karaman M (2005) Evaluation of pathological changes in broilers during chronic aflatoxin (50 and 100 ppb) and clinoptilolite exposure Res Vet Sci 78:61-68 doi:10.1016/j. rvsc.2004.06.006.

Peng X, Bai S, Ding X, Zeng Q, Zhang K, Fang J (2015) Pathological changes in the immune organs of broiler chickens fed on corn naturally contaminated with aflatoxins B1 and B2 Avian Pathol 44:192-199. doi:10.1080/03079457.2015.1023179.

Peng X et al. (2016) The mitochondrial and death receptor pathways involved in the thymocytes apoptosis induced by aflatoxin B1 Oncotarget 7:12222-12234 doi:10.18632/oncotarget.7731.

Peng X et al. (2014) Histological lesions, cell cycle arrest, apoptosis and T cell subsets changes of spleen in chicken fed aflatoxin-contaminated corn International journal of environmental research and public health 11:8567-8580 doi:10.3390/ijerph110808567.

Qureshi MA, Hagler WM (1992) Effect of Fumonisin-B1 Exposure on Chicken Macrophage Functions in vitro Poultry Sci 71:104-112. doi:10.3382/ps.0710104.

Raisuddin, Singh KP, Zaidi SIA, Saxena AK, Ray PK (1990) Effects of aflatoxin on lymphoid cells of weanling rat Journal of Applied Toxicology 10:245-250 doi:10.1002/jat.2550100404.

Raju MVLN, Devegowda G (2000) Influence of esterified-glucomannan on performance and organ morphology, serum biochemistry and haematology in broilers exposed to individual and combined mycotoxicosis (aflatoxin, ochratoxin and T-2 toxin) British poultry science 41:640-650 doi:10.1080/713654986.

Reed LJ, Muench H (1938) A Simple Method of Estimating Fifty Per Cent Endpoints12 American Journal of Epidemiology 27:493-497. doi:10.1093/oxfordjournals.aje.a118408.

Safamehr A (2008) The Performance and Heamatological Characters in Broiler Chicks Fed Ammonia-Treated Aflatoxin Contaminated Feed Journal of Animal and Veterinary Advances 7:331-336.

Salaberria C, Muriel J, de Luna M, Gil D, Puerta M (2013) The PHA test as an indicator of phagocytic activity in a passerine bird PLoS One 8:e84108 doi:10.1371/journal.pone.0084108.

Somayeh Asadzadeh M (2011) Detection of H9N2 avian influenza virus in various organs of experimentally infected chickens Afr J Microbiol Res 5 doi:10.5897/ajmr11.214.

Subler KA, Mickael CS, Jackwood DJ (2006) Infectious Bursal Disease Virus-Induced Immunosuppression Exacerbates Campylobacter jejuni Colonization and Shedding in Chickens Avian Dis 50:179-184. doi:10.1637/7434-090705r.1.

Sur E, Celik I (2003) Effects 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 doi:10.1080/000716603. 10001618352.

Theumer MG, Cánepa MC, López AG, Mary VS, Dambolena JS, Rubinstein HR (2010) Subchronic mycotoxicoses in Wistar rats: Assessment of the in vivo and in vitro genotoxicity induced by fumonisins and aflatoxin B1, and oxidative stress biomarkers status Toxicology 268:104-110 doi:10.1016/j.tox.2009.12.007.

Umar S, Arshad A, Ahmad B, Arshad M (2012) Clinic-biochemical and haematological changes in broilers induced by concurrent exposure to aflatoxin b1 and ochratoxin Journal of Public Health and Biological Sciences 1:79-85.

Umar S et al. (2015) Role of aflatoxin toxicity on transmissibility and pathogenicity of H9N2 avian influenza virus in turkeys Avian Pathol 44:305-310 doi:10.1080/03079457.2015.1046813.

Verma J, Johri TS, Swain BK, Ameena S (2010) Effect of graded levels of aflatoxin, ochratoxin and their combinations on the performance and immune response of broilers British poultry science 45:512-518 doi:10.1080/00071660412331286226.

Wells MA, Ennis FA, Albrecht P (1981) Recovery from a viral respiratory infection. II. Passive transfer of immune spleen cells to mice with influenza pneumonia J Immunol 126:1042-1046.

West S, Wyatt RD, Hamilton PB (1973) Improved yield of aflatoxin by incremental increases of temperature Appl Microbiol 25:1018-1019.

WHO (2002) WHO manual on animal influenza diagnosis and surveillance. Deptartment of Epidemic and Pandemic Alert and Response, Geneva, World Health Organization.

Wright S, Ramos R, Tobias P, Ulevitch R, Mathison J (1990) CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein Science 249:1431-1433 doi:10.1126/science.1698311.

Yuan S et al. (2016) The mitochondrial and endoplasmic reticulum pathways involved in the apoptosis of bursa of Fabricius cells in broilers exposed to dietary aflatoxin B1 Oncotarget 7:65295-65306 . doi:10.18632/oncotarget.11321.

Yunus AW, Razzazi-Fazeli E, Bohm J (2011) Aflatoxin B(1) in affecting broiler’s performance, immunity, and gastrointestinal tract: a review of history and contemporary issues Toxins (Basel) 3:566-590. doi:10.3390/toxins3060566.


Refbacks

  • There are currently no refbacks.


Copyright (c) 2020 H.F. ELLAKANY, H.S. ABD-ELHAMID, L.A. TANTAWY, H.A. ELSAMADONY, A.R. ELBESTAWY, A.R. GADO, Y.S. EL-SAYED, H.S. ISMAEL

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.