The effect of garlic (Allium sativum) and red onion (Allium cepa) on the histopathological signs of avian influenza disease in broiler chickens exposed to avian influenza virus subtype H9N2
Subject Areas :
Veterinary Clinical Pathology
Zolfaghar Rajabi
1
(Associate Professor, Department of Clinical Sciences, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.)
Amir Ali Shabazfar
2
(Associate Professor, Department of Pathobiology, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.)
Sadegh Haghparast kisami
3
(D.V.M. Graduate, Department of Clinical Sciences, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.)
Received: 2021-04-25
Accepted : 2021-08-23
Published : 2021-07-23
Keywords:
chickens,
Garlic,
onion,
Histopathology,
Influenza,
Abstract :
Avian Influenza (AI) virus subtype H9N2 is endemic in Iran and reported from all over the world. It causes economic losses to the poultry industry. In this study the role of garlic (Allium sativum) and red onion (Allium cepa) in reducing the severity of the histopathological signs of the avian influenza disease caused by subtype H9N2 in broiler chickens was evaluated. Toxicity of garlic and onion was evaluated first, and then the treatment groups consisting of 72 one day old Ross broiler chicks divided into 9 treatment groups were challenged with the H9N2 virus at 28 days. After one day, the challenged groups received garlic and red onion with feed for seven days. During the study, antibody titers against the H9N2 virus, clinical signs, and histopathological samples were recorded. The garlic and onion had no toxic effect on chickens. In histopathology, the percentage of goblet cells and villus diameter was statistically higher in negative control and treatment groups compared to the positive control group (p<0.05). It seems the garlic and red onion reduced the severity of the histopathological signs of the AI disease caused by subtype H9N2 in the duodenum of the broiler chickens. They are likely to play a role in repairing intestinal mucosa, by reducing the number of the viruses.
References:
Aghahossein, F.A., Barin, A., Moosakhani, F. and Ghalyanchi, L.A. (2012). Genetical Evaluation of resistance to amantadine in H9N2 Avian influenza virus in Iran between1998 to 2009. Veterinary Clinical Pathology, 5(4): 1387-1395. [In Persian]
Ahmadi, S., Rajabi, Z. and Marandi, M.V. (2018). Evaluation of the antiviral effects of aqueous extracts of red and yellow onions (Allium cepa) against avian influenza virus subtype H9N2. Iranian Journal of Science and Technology, 8(9): 23-27.
Ahmed, I., Aslam, A., Mustafa, G., Masood, S., Ali, M.A. and Nawaz, M. (2017). Anti-avian influenza virus H9N2 activity of aqueous extracts of Zingiber officinalis (Ginger) and Allium sativum (Garlic) in chick embryos. Pakistan Journal of Pharmaceutical Sciences, 30(4): 1341-1344.
Alagawany, M., Elnesr, S.S., Farag, M.R., El, H.A., Mohamed, E., Khafaga, A.F., et al. (2019). Use of licorice (Glycyrrhiza glabra) herb as a feed additive in poultry: Current knowledge and prospects. Animals, 9(8): 536-546.
Al-Garib, S., Agha, A. and Al-Mesilaty, L. (2016). Low pathogenic avian influenza H9N2: world-wide distribution. World's Poultry Science Journal, 72(1): 125-136.
Balzarini, J. (2006). Inhibition of HIV entry by carbohydrate-binding proteins. Antiviral Research, 71(2-3): 237-247.
Bayan, L., Koulivand, P.H. and Gorji, A. (2014). Garlic: a review of potential therapeutic effects. Avicenna Journal of Phytomedicine, 4(1): 1-14.
Brüll, V., Burak, C., Stoffel, W.B., Wolffram, S., Nickenig, G., Müller, C., et al. (2015). Effects of a quercetin-rich onion skin extract on 24 h ambulatory blood pressure and endothelial function in overweight-to-obese patients with (pre-) hypertension: a randomised double-blinded placebo-controlled cross-over trial. British Journal of Nutrition, 114(8): 1263-1277.
Chung, L.Y. (2006). The antioxidant properties of garlic compounds: allyl cysteine, alliin, allicin, and allyl disulfide. Journal of Medicinal Food, 9(2): 205-213.
De, V.H., Mignon, G.S., Jeulin, C., Le, B.D.E., Leconte, M., Mallet, S., et al. (2010). Digestive tract measurements and histological adaptation in broiler lines divergently selected for digestive efficiency. Poultry Science, 89(9): 1955-1961.
Hosseini, A. and Hosseinzadeh, H. (2015). A review on the effects of Allium sativum (Garlic) in metabolic syndrome. Journal of Endocrinological Investigation, 38(11): 1147-1157.
Faramarzi, S. and Khaki, A. (2015). Study on the effects of essential oil of Thymus vulgaris after administration of the LaSota vaccine on histopathological status of the trachea, humoral immune system and the performance of broilers. Veterinary Clinical Pathology, 9(3): 191-204. [In Persian]
Fathihafshanjani, E. (2013). Survey of primultaneous Contamination with CIAV and infection with AI and ND in broiler chicken of Chaharmahal-va-Bakhtiari Provence. Veterinary Clinical Pathology, 7(1): 1762-1772. [In Persian]
Hussein, H.J., Hameed, I.H. and Hadi, M.Y. (2017). A review: Anti-microbial, anti-inflammatory effect and cardiovascular effects of garlic: Research Journal of Pharmacy and Technology, 10(11): 4069-4078.
Jaiswal, N. and Rizvi, S.I. (2014). Onion extract (Allium cepa L.), quercetin and catechin up‐regulate paraoxonase 1 activity with concomitant protection against low‐density lipoprotein oxidation in male Wistar rats subjected to oxidative stress. Journal of the Science of Food and Agriculture, 94(13): 2752-2757.
Karimi, S., Mohammadi, A. and Dadras, H. (2014). The effect of Echinacea purpurea and Sambucusnigra L. on H9N2 avian influenza virus in infected chicken embryo. Veterinarski Arhiv, 84(2): 153-165.
Kavalcová, P., Bystrická, J., Tomáš, J., Karovičová, J. and Kuchtová, V. (2014). Evaluation and comparison of the content of total polyphenols and antioxidant activity in onion, garlic and leek. Potravinarstvo Slovak Journal of Food Sciences, 8(1): 272-276.
Khan, S.U., Anderson, B.D., Heil, G.L., Liang, S. and Gray, G.C. (2015). A systematic review and meta-analysis of the seroprevalence of influenza A (H9N2) infection among humans. The Journal of infectious diseases, 212(4): 562-569.
Khonsary, S. A. (2017). Textbook of medical physiology. Surgical neurology international. 13th ed., Elsevier, Hardcover. pp: 797-853.
Killian, M.L. (2008). Hemagglutination assay for the avian influenza virus. In: Avian influenza virus. 1th ed. Humana Press. pp: 47-52.
Landmann, M., Scheibner, D., Graaf, A., Gischke, M., Koethe, S., Fatola, O.I., et al. (2021). A Semiquantitative Scoring System for Histopathological and Immunohistochemical Assessment of Lesions and Tissue Tropism in Avian Influenza. Viruses, 13(5): 868-897.
Mahomoodally, F., Ramcharun, S. and Zengin, G. (2018). Onion and Garlic Extracts Potentiate the Efficacy of Conventional Antibiotics against Standard and Clinical Bacterial Isolates. Current Topics in Medicinal Chemistry, 18(9): 787-796.
Milewski, L.M. and Khan, S.A. (2006). An overview of potentially life‐threatening poisonous plants in dogs and cats. Journal of Veterinary Emergency and Critical Care, 16(1): 25-33.
Mollavali, M., Bolandnazar, S.A., Schwarz, D., Rohn, S., Riehle, P. and Zaare Nahandi, F. (2016). Flavonol glucoside and antioxidant enzyme biosynthesis affected by mycorrhizal fungi in various cultivars of onion (Allium cepa L.). Journal of Agricultural and Food Chemistry, 64(1): 71-77.
Nili, H. and Asasi, K. (2002). Natural cases and an experimental study of H9N2 avian influenza in commercial broiler chickens of Iran. Avian Pathology, 31(3): 247-252.
Nili, H. and Asasi, K. (2003). Avian influenza (H9N2) outbreak in Iran. Avian Diseases, 47(s3): 828-831.
Noda, T. and Kawaoka, Y. (2010). Structure of influenza virus ribonucleoprotein complexes and their packaging into virions. Reviews in Medical Virology, 20(6): 380-391.
Park, K.Y., Jeong, J.K., Lee, Y.E. and Daily, J.W. (2014). Health benefits of kimchi (Korean fermented vegetables) as a probiotic food. Journal of Medicinal Food, 17(1): 6-20.
Pazani, J., Marandi, M.V., Ashrafihelan, J., Marjanmehr, S.H. and Ghods, F. (2008). Pathological studies of A/Chicken/Tehran/ZMT-173/99 (H9N2) influenza virus in commercial broiler chickens of Iran. International Journal of Poultry Science, 7(5): 502-510.
Perkins, L.E.L. and Swayne, D.E. (2001). Pathobiology of A/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Veterinary Pathology, 38(2): 149-164.
Pinto, L.H. and Lamb, R.A. (2006). The M2 proton channels of influenza A and B viruses. Journal of Biological Chemistry, 281(14): 8997-9000.
Ramirez, J., Guarner, F., Bustos Fernandez, L., Maruy, A., Sdepanian, V.L. and Cohen, H. (2020). Antibiotics as Major Disruptors of Gut Microbiota. Frontiers in Cellular and Infection Microbiology, 11(10): 731-740.
Santoyo, S., Jaime, L., García-Risco, M.R., Lopez-Hazas, M. and Reglero, G. (2014). Supercritical fluid extraction as an alternative process to obtain antiviral agents from thyme species. Industrial Crops and Products, 52(1): 475-480.
Shalini, R., Abinaya, G., Saranya, P. and Antony, U. (2017). Growth of selected probiotic bacterial strains with fructans from Nendran banana and garlic. LWT-Food Science and Technology, 83(9): 68-78.
Sobenin, I.A., Andrianova, I.V., Lakunin, K.Y., Karagodin, V.P., Bobryshev, Y.V. and Orekhov, A.N. (2016). Anti-atherosclerotic effects of garlic preparation in freeze injury model of atherosclerosis in cholesterol-fed rabbits. Phytomedicine, 23(11): 1235-1239.
Swayne, D.E., Suarez, D.L. and Sims, D.L. (2020). Influenza. In: Disease of poultry. Swayne, D.E., Boulianne, M., Logue, C.M., McDougall, L.R., Nair, V., Suarez, D.L. editors.14th ed., UK: London, Blackwell Sciences Ltd. pp: 210-252.
Talat, S., Abouelmaatti, R.R., Almeer, R., Abdel, D.M.M. and Elfeil, W.K. (2020). Comparison of the effectiveness of two different vaccination regimes for avian influenza H9N2 in broiler chicken. Animals, 10(10): 1875.
Tavakkoli, H., Asasi, K. and Mohammadi, A. (2011). Effectiveness of two H9N2 low pathogenic avian influenza conventional inactivated oil emulsion vaccines on H9N2 viral replication and shedding in broiler chickens. Iranian Journal of Veterinary Research, 12(3): 214-221.
Vasfi, M.M. and Bozorg, M.M. (2002). Isolation of H9N2 subtype of avian influenza viruses during an outbreak in chickens in Iran. Iranian Biomedical Journal, 6(1): 13-7.
Villegas, P. (2008). Titration of biological suspensions. In: Laboratory manual for the isolation and identification of avian pathogens. Dufour-Za, L., Swayne, D.E., Glisson, J.R., Pearson, J.E., Reed, W.M., Jackwood, M.W. and Woolcock, P.R. editors. 5th ed., USA: American Association of Avian Pathologists, University of Pennsylvania, pp: 217-221.
Wainright, P.O., Perdue, M.L., Brugh, M. and Beard, C.W. (1991). Amantadine resistance among hemagglutinin subtype 5 strains of avian influenza virus. Avian Diseases, 35(1): 31-39.
Wang, Y., Li, C., Xiang, L., Huang, W. and He, X. (2016). Spirostanol saponins from Chinese onion (Allium chinense) exert pronounced anti-inflammatory and anti-proliferative activities. Journal of Functional Foods, 25(8): 208-219.
Woolcock, P.R. (2008). Avian influenza virus isolation and propagation in chicken eggs. In: Avian Influenza Virus. 1th ed., Humana Press. pp: 35-46.
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Aghahossein, F.A., Barin, A., Moosakhani, F. and Ghalyanchi, L.A. (2012). Genetical Evaluation of resistance to amantadine in H9N2 Avian influenza virus in Iran between1998 to 2009. Veterinary Clinical Pathology, 5(4): 1387-1395. [In Persian]
Ahmadi, S., Rajabi, Z. and Marandi, M.V. (2018). Evaluation of the antiviral effects of aqueous extracts of red and yellow onions (Allium cepa) against avian influenza virus subtype H9N2. Iranian Journal of Science and Technology, 8(9): 23-27.
Ahmed, I., Aslam, A., Mustafa, G., Masood, S., Ali, M.A. and Nawaz, M. (2017). Anti-avian influenza virus H9N2 activity of aqueous extracts of Zingiber officinalis (Ginger) and Allium sativum (Garlic) in chick embryos. Pakistan Journal of Pharmaceutical Sciences, 30(4): 1341-1344.
Alagawany, M., Elnesr, S.S., Farag, M.R., El, H.A., Mohamed, E., Khafaga, A.F., et al. (2019). Use of licorice (Glycyrrhiza glabra) herb as a feed additive in poultry: Current knowledge and prospects. Animals, 9(8): 536-546.
Al-Garib, S., Agha, A. and Al-Mesilaty, L. (2016). Low pathogenic avian influenza H9N2: world-wide distribution. World's Poultry Science Journal, 72(1): 125-136.
Balzarini, J. (2006). Inhibition of HIV entry by carbohydrate-binding proteins. Antiviral Research, 71(2-3): 237-247.
Bayan, L., Koulivand, P.H. and Gorji, A. (2014). Garlic: a review of potential therapeutic effects. Avicenna Journal of Phytomedicine, 4(1): 1-14.
Brüll, V., Burak, C., Stoffel, W.B., Wolffram, S., Nickenig, G., Müller, C., et al. (2015). Effects of a quercetin-rich onion skin extract on 24 h ambulatory blood pressure and endothelial function in overweight-to-obese patients with (pre-) hypertension: a randomised double-blinded placebo-controlled cross-over trial. British Journal of Nutrition, 114(8): 1263-1277.
Chung, L.Y. (2006). The antioxidant properties of garlic compounds: allyl cysteine, alliin, allicin, and allyl disulfide. Journal of Medicinal Food, 9(2): 205-213.
De, V.H., Mignon, G.S., Jeulin, C., Le, B.D.E., Leconte, M., Mallet, S., et al. (2010). Digestive tract measurements and histological adaptation in broiler lines divergently selected for digestive efficiency. Poultry Science, 89(9): 1955-1961.
Hosseini, A. and Hosseinzadeh, H. (2015). A review on the effects of Allium sativum (Garlic) in metabolic syndrome. Journal of Endocrinological Investigation, 38(11): 1147-1157.
Faramarzi, S. and Khaki, A. (2015). Study on the effects of essential oil of Thymus vulgaris after administration of the LaSota vaccine on histopathological status of the trachea, humoral immune system and the performance of broilers. Veterinary Clinical Pathology, 9(3): 191-204. [In Persian]
Fathihafshanjani, E. (2013). Survey of primultaneous Contamination with CIAV and infection with AI and ND in broiler chicken of Chaharmahal-va-Bakhtiari Provence. Veterinary Clinical Pathology, 7(1): 1762-1772. [In Persian]
Hussein, H.J., Hameed, I.H. and Hadi, M.Y. (2017). A review: Anti-microbial, anti-inflammatory effect and cardiovascular effects of garlic: Research Journal of Pharmacy and Technology, 10(11): 4069-4078.
Jaiswal, N. and Rizvi, S.I. (2014). Onion extract (Allium cepa L.), quercetin and catechin up‐regulate paraoxonase 1 activity with concomitant protection against low‐density lipoprotein oxidation in male Wistar rats subjected to oxidative stress. Journal of the Science of Food and Agriculture, 94(13): 2752-2757.
Karimi, S., Mohammadi, A. and Dadras, H. (2014). The effect of Echinacea purpurea and Sambucusnigra L. on H9N2 avian influenza virus in infected chicken embryo. Veterinarski Arhiv, 84(2): 153-165.
Kavalcová, P., Bystrická, J., Tomáš, J., Karovičová, J. and Kuchtová, V. (2014). Evaluation and comparison of the content of total polyphenols and antioxidant activity in onion, garlic and leek. Potravinarstvo Slovak Journal of Food Sciences, 8(1): 272-276.
Khan, S.U., Anderson, B.D., Heil, G.L., Liang, S. and Gray, G.C. (2015). A systematic review and meta-analysis of the seroprevalence of influenza A (H9N2) infection among humans. The Journal of infectious diseases, 212(4): 562-569.
Khonsary, S. A. (2017). Textbook of medical physiology. Surgical neurology international. 13th ed., Elsevier, Hardcover. pp: 797-853.
Killian, M.L. (2008). Hemagglutination assay for the avian influenza virus. In: Avian influenza virus. 1th ed. Humana Press. pp: 47-52.
Landmann, M., Scheibner, D., Graaf, A., Gischke, M., Koethe, S., Fatola, O.I., et al. (2021). A Semiquantitative Scoring System for Histopathological and Immunohistochemical Assessment of Lesions and Tissue Tropism in Avian Influenza. Viruses, 13(5): 868-897.
Mahomoodally, F., Ramcharun, S. and Zengin, G. (2018). Onion and Garlic Extracts Potentiate the Efficacy of Conventional Antibiotics against Standard and Clinical Bacterial Isolates. Current Topics in Medicinal Chemistry, 18(9): 787-796.
Milewski, L.M. and Khan, S.A. (2006). An overview of potentially life‐threatening poisonous plants in dogs and cats. Journal of Veterinary Emergency and Critical Care, 16(1): 25-33.
Mollavali, M., Bolandnazar, S.A., Schwarz, D., Rohn, S., Riehle, P. and Zaare Nahandi, F. (2016). Flavonol glucoside and antioxidant enzyme biosynthesis affected by mycorrhizal fungi in various cultivars of onion (Allium cepa L.). Journal of Agricultural and Food Chemistry, 64(1): 71-77.
Nili, H. and Asasi, K. (2002). Natural cases and an experimental study of H9N2 avian influenza in commercial broiler chickens of Iran. Avian Pathology, 31(3): 247-252.
Nili, H. and Asasi, K. (2003). Avian influenza (H9N2) outbreak in Iran. Avian Diseases, 47(s3): 828-831.
Noda, T. and Kawaoka, Y. (2010). Structure of influenza virus ribonucleoprotein complexes and their packaging into virions. Reviews in Medical Virology, 20(6): 380-391.
Park, K.Y., Jeong, J.K., Lee, Y.E. and Daily, J.W. (2014). Health benefits of kimchi (Korean fermented vegetables) as a probiotic food. Journal of Medicinal Food, 17(1): 6-20.
Pazani, J., Marandi, M.V., Ashrafihelan, J., Marjanmehr, S.H. and Ghods, F. (2008). Pathological studies of A/Chicken/Tehran/ZMT-173/99 (H9N2) influenza virus in commercial broiler chickens of Iran. International Journal of Poultry Science, 7(5): 502-510.
Perkins, L.E.L. and Swayne, D.E. (2001). Pathobiology of A/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Veterinary Pathology, 38(2): 149-164.
Pinto, L.H. and Lamb, R.A. (2006). The M2 proton channels of influenza A and B viruses. Journal of Biological Chemistry, 281(14): 8997-9000.
Ramirez, J., Guarner, F., Bustos Fernandez, L., Maruy, A., Sdepanian, V.L. and Cohen, H. (2020). Antibiotics as Major Disruptors of Gut Microbiota. Frontiers in Cellular and Infection Microbiology, 11(10): 731-740.
Santoyo, S., Jaime, L., García-Risco, M.R., Lopez-Hazas, M. and Reglero, G. (2014). Supercritical fluid extraction as an alternative process to obtain antiviral agents from thyme species. Industrial Crops and Products, 52(1): 475-480.
Shalini, R., Abinaya, G., Saranya, P. and Antony, U. (2017). Growth of selected probiotic bacterial strains with fructans from Nendran banana and garlic. LWT-Food Science and Technology, 83(9): 68-78.
Sobenin, I.A., Andrianova, I.V., Lakunin, K.Y., Karagodin, V.P., Bobryshev, Y.V. and Orekhov, A.N. (2016). Anti-atherosclerotic effects of garlic preparation in freeze injury model of atherosclerosis in cholesterol-fed rabbits. Phytomedicine, 23(11): 1235-1239.
Swayne, D.E., Suarez, D.L. and Sims, D.L. (2020). Influenza. In: Disease of poultry. Swayne, D.E., Boulianne, M., Logue, C.M., McDougall, L.R., Nair, V., Suarez, D.L. editors.14th ed., UK: London, Blackwell Sciences Ltd. pp: 210-252.
Talat, S., Abouelmaatti, R.R., Almeer, R., Abdel, D.M.M. and Elfeil, W.K. (2020). Comparison of the effectiveness of two different vaccination regimes for avian influenza H9N2 in broiler chicken. Animals, 10(10): 1875.
Tavakkoli, H., Asasi, K. and Mohammadi, A. (2011). Effectiveness of two H9N2 low pathogenic avian influenza conventional inactivated oil emulsion vaccines on H9N2 viral replication and shedding in broiler chickens. Iranian Journal of Veterinary Research, 12(3): 214-221.
Vasfi, M.M. and Bozorg, M.M. (2002). Isolation of H9N2 subtype of avian influenza viruses during an outbreak in chickens in Iran. Iranian Biomedical Journal, 6(1): 13-7.
Villegas, P. (2008). Titration of biological suspensions. In: Laboratory manual for the isolation and identification of avian pathogens. Dufour-Za, L., Swayne, D.E., Glisson, J.R., Pearson, J.E., Reed, W.M., Jackwood, M.W. and Woolcock, P.R. editors. 5th ed., USA: American Association of Avian Pathologists, University of Pennsylvania, pp: 217-221.
Wainright, P.O., Perdue, M.L., Brugh, M. and Beard, C.W. (1991). Amantadine resistance among hemagglutinin subtype 5 strains of avian influenza virus. Avian Diseases, 35(1): 31-39.
Wang, Y., Li, C., Xiang, L., Huang, W. and He, X. (2016). Spirostanol saponins from Chinese onion (Allium chinense) exert pronounced anti-inflammatory and anti-proliferative activities. Journal of Functional Foods, 25(8): 208-219.
Woolcock, P.R. (2008). Avian influenza virus isolation and propagation in chicken eggs. In: Avian Influenza Virus. 1th ed., Humana Press. pp: 35-46.
