Herbal Medicine Additives as Powerful Agents to Control and Prevent Avian Influenza Virus in Poultry – A Review

Abbas A., Abbas R.Z., Masood S., Iqbal Z., Khan M.K., Saleemi M.K., Raza M.A., Mahmood M.S., Khan J.A., Sindhu Z.D. (2018). Acaricidal and insecticidal effects of essential oils against ectoparasites of veterinary importance. BLACPMA, 17: 441–452.Search in Google Scholar

Abd El-Hack M.E., Mahgoub S.A., Alagawany M., Dhama K. (2015). Influences of dietary supplementation of antimicrobial cold pressed oils mixture on growth performance and intestinal microflora of growing Japanese quails. Int. J. Pharmacol., 11: 689–696.10.3923/ijp.2015.689.696Search in Google Scholar

Abd El-Hack M.E., Alagawany M., Farag M.R., Tiwari R., Karthik K., Dhama K., Zorriehzahra J., Adel M. (2016). Beneficial impacts of thymol essential oil on health and production of animals, fish and poultry: A review. J. Essential Oil Res., 28: 365–382.10.1080/10412905.2016.1153002Search in Google Scholar

Abd El-Hack M.E., Mahgoub S.A., Hussein M.M., Saadeldin I.M. (2018). Improving growth performance and health status of meat-type quail by supplementing the diet with black cumin cold-pressed oil as a natural alternative for antibiotics. Environ. Sci. Poult. Res., 25: 1157–1167.10.1007/s11356-017-0514-0Search in Google Scholar

Abd El-Hack M.E., Abdelnour S.A., Taha A.E., Khafaga A.F., Arif M., Ayasan T., Abdel-Daim M.M. (2019). Herbs as thermoregulatory agents in poultry: An overview. Sci. Total Environ., 134399.10.1016/j.scitotenv.2019.134399Search in Google Scholar

Abd El-Hamid H.S., Ellakany H.F., Elbestawy A.R., Seliem A.A., Khalil H.S. (2018). In vitro antiviral activity of commercial products of herbal extracts against highly pathogenic avian influenza (H5N1) virus. Alexandria J. Vet. Sci., 56: 145–152.10.5455/ajvs.281430Search in Google Scholar

Abdelnour S.A., Abd El-Hack M.E., Arif M., Khafaga A.F., Taha A.E. (2019). The application of Chlorella microalgae as a feed supplement in broiler feed. Word’s Poultry Sci., 75: 305–318.10.1017/S0043933919000047Search in Google Scholar

Abdelwhab E.M., Hafez H.M. (2012). Insight into alternative approaches for control of avian influenza in poultry, with emphasis on highly pathogenic H5N1. Viruses, 4: 3179–3208.10.3390/v4113179Search in Google Scholar

Abdullahi A., Kallon S., Yu X., Yongliang Z., Guoqing L. (2016). Vaccination with astragalus and ginseng polysaccharides improves immune response of chickens against H5N1 avian influenza virus. Biomed. Res. Int., Doi: 8.10.1155/2016/1510264.10.1155/2016/1510264500247727597953Open DOISearch in Google Scholar

Alagawany M., Abd El-Hack M.E., Farag M.R., Sachan S., Karthik K., Khama K. (2018). The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environ. Sci. Poult. Res., 25: 10611–11618.10.1007/s11356-018-1687-xSearch in Google Scholar

Alagawany M., Elnesr S.S., Farag M.R., Abd El-Hack M.E., Khafaga A.F., Taha A.E., Tiwari R., Yatoo M.I., Bhatt P., Marappan G., Dhama K. (2019). Licorice (Glycyrrhiza glabra) herb as an eco-fiendly additive to promote poultry health – current knowledge and prospects. Animals, 9: 536.10.3390/ani9080536Search in Google Scholar

Awaad M.H.H., Abdel-Alim G.A., Sayed K.S.S., Ahmed K.A., Nada A.A., Metwalli A.S.Z., Alkhalaf A.N. (2010). Immunostimulant effects of essential oils of peppermint and eucalyptus in chickens. Pakistan Vet. J., 30: 61–66.Search in Google Scholar

Babaei S., Rahimi S., Torshizi M.A.K., Tahmasebi G., Seyed N.K.M. (2016). Effects of propolis, royal jelly, honey and bee pollen on growth performance and immune system of Japanese quails. Vet. Res. Forum, 7: 13–20.Search in Google Scholar

Barbour E., Ryan H.Y., Lina J., Houssam S., Steve H. (2010) Safety and antiviral activity of essential oil against avian influenza and Newcastle disease viruses. Int. J. Appl. Res. Vet. Med., 8: 60–64.Search in Google Scholar

Bertelsen M.F., Klausen J., Holm E., Grondahl C., Jorgensen P.H. (2007). Serological response to vaccination against avian influenza in zoo-birds using an inactivated H5N9 vaccine. Vaccine, 25: 4345–4349.10.1016/j.vaccine.2007.03.043Search in Google Scholar

Boni M.F. (2008). Vaccination and antigenic drift in influenza. Vaccine, 26: C8–14.10.1016/j.vaccine.2008.04.011Search in Google Scholar

Busani L., Toson M., Stegeman A., Pozza M.D., Comin A., Mulatti P., Mattia C., Stefano M. (2009). Vaccination reduced the incidence of outbreaks of low pathogenicity avian influenza in northern Italy. Vaccine, 27: 3655–3661.10.1016/j.vaccine.2009.03.033Search in Google Scholar

Cagle C., To T.L., Nguyen T., Wasilenko J., Adams S.C., Cardona C.J., Spackman E., Suarez D.L., Pantin-Jackwood M.J. (2011). Pekin and Muscovy ducks respond differently to vaccination with a H5N1 highly pathogenic avian influenza (HPAI) commercial inactivated vaccine. Vaccine, 29: 6549–6557.10.1016/j.vaccine.2011.07.004Search in Google Scholar

Capua I., Schmitz A., Jestin V., Koch G., Maragon S. (2009). Vaccination as a tool to combat introductions of notifiable avian influenza viruses in Europe, 2000 to 2006. Rev. Sci. Tech., 28: 245–259.10.20506/rst.28.1.1861Search in Google Scholar

Cattoli G., Fusaro A., Monne I., Coven F., Joannis T., El-Hamid H.S., Hussein A.A., Cornelius C., Amarin N.M., Mancin M., Holmes E.C., Capua I. (2011 a). Evidence for differing evolutionary dynamics of A/H5N1 viruses among countries applying or not applying avian influenza vaccination in poultry. Vaccine, 29: 9368–9375.10.1016/j.vaccine.2011.09.12722001877Search in Google Scholar

Cattoli A., Milani A., Temperton N., Zecchin B., Buratin A., Molesti E., Aly M.M., Arafa A., Capua I. (2011 b). Antigenic drift in H5N1 avian influenza virus in poultry is driven by mutations in major antigenic sites of the hemagglutinin molecule analogous to those for human influenza virus. Virology, 85: 8718–8724.10.1128/JVI.02403-10316583721734057Search in Google Scholar

Cheng P.W., Chiang L.C., Yen M.H., Lin C.C. (2007). Bupleurum kaoi inhibits Coxsackie B virus type 1 infection of CCFS-1 cells by induction of type I interferons expression. Food Chem. Toxicol., 45: 24–31.10.1016/j.fct.2006.06.007Search in Google Scholar

De Vriese J., Steensels M., Palya V., Gardin Y., Dorsey K.M., Lambrecht B., Van Borm S., Vanden Berg T. (2010). Passive protection afforded by maternally-derived antibodies in chickens and the antibodies' interference with the protection elicited by avian influenza-inactivated vaccines in progeny. Avian Dis., 54: 246–52.10.1637/8908-043009-Reg.1Search in Google Scholar

Dehkordi S.H., Fallah V. (2011). Enhancement of broiler performance and immune response by Echinacea purpurea supplemented in diet. Afr. J. Biotechnol., 10: 11280–11286.10.5897/AJB11.1484Search in Google Scholar

Dhingra M.S., Artois J., Dellicour S., Lemey P., Dauphin G., Von Dobschuetz S., Van Boeckel T.P., Castellan D.M., Morzaria S., Gilbert M. (2018). Geographical and historical patterns in the emergences of novel highly pathogenic avian influenza (HPAI) H5 and H7 viruses in poultry. Front. Vet. Sci., https://doi.org/10.3389/fvets.2018.0008410.3389/fvets.2018.00084599608729922681Open DOISearch in Google Scholar

Ebrahimi A., Santini A., Alise M., Pourhossein Z., Miraalami N., Seidavi A. (2015). Effect of dried Citrus sinensis peel on gastrointestinal microbiota and immune system traits of broiler chickens. It. J. Anim. Sci., 14: 4194.10.4081/ijas.2015.4194Search in Google Scholar

Eid K.M., Iraqi M.M. (2014). Effect of garlic powder on growth performance and immune response for Newcastle and avian influenza virus diseases in broiler of chickens. Proc. 2nd International Conference Biotechnology Applications in Agriculture (ICBAA), Benha University, Moshtohor and Hurghada, pp. 8–12.Search in Google Scholar

Escorcia M., Vázquez L., Méndez S.T., Rodríguez-Ropón A., Lucio E., Nava G.M. (2008). Avian influenza: genetic evolution under vaccination pressure. Virol. J., 5: 15. https://doi.org/10.1186/1743–422X–5-15.10.1186/1743422X5-15Open DOISearch in Google Scholar

Fallah R. (2014). Effects of supplementing Aloe vera gel and garlic powder on blood biochemical parameters and immune response of broiler. J. Med. Plant Res., 8: 32. Doi: 10.5897/JMPR2014.5521.10.5897/JMPR2014.5521Open DOISearch in Google Scholar

Fallah R., Mirzaei E. (2016). Effect of dietary inclusion of turmeric and thyme powders on performance, blood parameters and immune system of broiler chickens. J. Livest. Sci., 7: 180–186.Search in Google Scholar

Fard S.H., Toghyani M., Tabeidian S.A. (2014). Effect of oyster mushroom wastes on performance, immune responses and intestinal morphology of broiler chickens. Int. J. Recyc. Org. Waste Agr., 3: 141–146.10.1007/s40093-014-0076-9Search in Google Scholar

Galal A.A., El-Araby I.E., Hassanin O., Omar A.E. (2016). Positive impact of oregano essential oil on growth performance, humoral immune responses and chicken interferon alpha signalling pathway in broilers. Adv. Anim. Vet. Sci., 4: 57–65.10.14737/journal.aavs/2016/4.1.57.65Search in Google Scholar

Ganjhu R.K., Mudgal P.P., Maity H., Dowarha D., Devadiga S., Nag S., Arunkuma G. (2015). Herbal plants and plant preparations as remedial approach for viral diseases. Virus Dis., 26: 225–236.10.1007/s13337-015-0276-6Search in Google Scholar

Ghalamkari G., Toghyani M., Tavalaeian E., Landy N., Ghalamkari Z., Radnezhad H. (2011). Efficiency of different levels of Satureja hortensis L. (Savory) in comparison with an antibiotic growth promoter on performance, carcass traits, immune responses and serum biochemical parameters in broiler chickens. Afr. J. Biotechnol., 10: 13318–13323.Search in Google Scholar

Gheisari A., Shahrvand S., Landy N. (2017). Effect of ethanolic extract of propolis as an alternative to antibiotics as a growth promoter on broiler performance, serum biochemistry, and immune responses. Vet. World, 10: 249–254.10.14202/vetworld.2017.249-254Search in Google Scholar

Goudarzi M., Samiei I., Nanekarani S., Nasrolahi F. (2016). The effect of Myrtus communis oil extract on growth performance and immune responses in Ross and Cobb strain broilers. J. Adv. Agr. Technol., 3: 1.10.18178/joaat.3.1.10-14Search in Google Scholar

Guo L., Wang D., Hu Y., Zhao X., Wang Y., Yang S., Wang J., Fan Y., Han G., Gao H. (2012). Adjuvanticity of compound polysaccharides on chickens against Newcastle disease and avian influenza vaccine. Int. J. Biol. Macromol., 50: 512–517.10.1016/j.ijbiomac.2012.01.002Search in Google Scholar

Hao Y.X., Yang J.M., He C., Liu Q., Mcallister T.A. (2008). Reduced serologic response to avian influenza vaccine in specific-pathogen-free chicks inoculated with Cryptosporidium Baileyi. Avian Dis., 52: 690–693.10.1637/8370-052608-Reg.1Search in Google Scholar

Hartati S., Untari T., Fitriyani I., Sutrisno B. (2015). Evaluation of immunomodulatory activity of the herbals formula viranur, turmeric (Curcuma heyneana Val.) and phyllanthus (Phyllanthus niruri L.) in layer chicken vaccinated with avian influenza. J. Agric. Sci. Technol., 5: 8.10.17265/2161-6256/2015.08.008Search in Google Scholar

He W., Han H., Wang W., Gao B. (2011). Anti-influenza virus effect of aqueous extracts from dandelion. Virol. J., 8: 538.10.1186/1743-422X-8-538Search in Google Scholar

Hegazy A.M., Abdallah F.M., Abd-El Samie L.K., Nazim A.A. (2011). The relation between some immunosuppressive agents and widespread nature of highly pathogenic avian influenza (HPAI) post vaccination. J. Am. Sci., 7: 66–72.Search in Google Scholar

Hosseinzadeh H., Qotbi A., Seidavi A., Norris D., Brown D. (2014). Effects of different levels of coriander (Coriandrum sativum) seed powder and extract on serum biochemical parameters, microbiota, and immunity in broiler chicks. Sci. World J., 2014: 628979.10.1155/2014/628979Search in Google Scholar

Jafari A., Ghorbanpoor M., Hoshmand D.S. (2009). Study on immunomodulatory activity of dietary garlic in chickens vaccinated against avian influenza virus (subtype H9N2). Int. J. Poultry Sci., 8: 401–403.10.3923/ijps.2009.401.403Search in Google Scholar

Jiang W., Liu Y., Zheng H., Zheng Y., Xu H., Lu H. (2012). Immune regulation of avian influenza vaccine in hens using Hypericum perforatum L. methanol extraction. Plant Omics, 5: 40–45.Search in Google Scholar

Kallon S., Abdullahi A.Y. (2015). Immunity against avian influenza viruspanax ginseng polysaccharide (GPS) can improve immunity against H9N2 avian influenza virus in chickens. Iran. J. Appl. Anim. Sci., 5: 715–722.Search in Google Scholar

Kallon S., Li X., Ji J., Xi Q., Ma J., Xie Q., Zhang Y. (2013). Astragalus polysaccharide enhances immunity and inhibits H9N2 avian influenza virus in vitro and in vivo. J. Anim. Sci. Biotechnol., 4: 22.10.1186/2049-1891-4-22Search in Google Scholar

Kapczynski D.R., Swayne D.E. (2009). Influenza vaccines for avian species. Curr. Top. Microbiol. Immunol., 333: 133–152.10.1007/978-3-540-92165-3_6Search in Google Scholar

Karimi S., Mohammadi A., Dadras H. (2014). The effect of Echinacea purpurea and Sambucus nigra L. on H9N2 avian influenza virus in infected chicken embryo. Vet. Arch., 84: 153–165.Search in Google Scholar

Karimi A., Majlesi M., Rafieian-Kopae M. (2015). Herbal versus synthetic drugs; beliefs and facts. J. Nephropharmacol., 4: 27–30.Search in Google Scholar

Khafaga A.F., Bayad A.E. (2016 a). Impact of Ginkgo biloba extract on reproductive toxicity induced by single or repeated injection of cisplatin in adult male rats. Int. J. Pharmacol., 12: 340–350.10.3923/ijp.2016.340.350Search in Google Scholar

Khafaga A.F., Bayad A.E. (2016 b). Ginkgo biloba extract attenuates hematological disorders, oxidative stress and nephrotoxicity induced by single or repeated injection cycles of cisplatin in rats: physiological and Pathological Studies. Asian J. Anim. Sci., 10: 235–246.10.3923/ajas.2016.235.246Search in Google Scholar

Khafaga A.F., El-Hack M.E.A., Taha A.E., Elnesr S.S., Alagawany M. (2019 a). The potential modulatory role of herbal additives against Cd toxicity in human, animal, and poultry: a review. Environ. Sci. Pollut. Res., 26: 4588–4604.10.1007/s11356-018-4037-030612355Search in Google Scholar

Khafaga A.F., Noreldin A.E., Taha A.E. (2019 b). The adaptogenic anti-ageing potential of resveratrol against heat stress-mediated liver injury in aged rats: Role of HSP70 and NF-kB signalling. J. Therm. Biol., 83: 8–21.10.1016/j.jtherbio.2019.04.01231331528Search in Google Scholar

Kim J., Kayali G., Walker D., Forrest H.L., Ellebedy H.A., Griffin Y.S., Rubrum A., Bahgat M.M., Kutkat M.A., Ali M.A.A., Aldridge J.R., Negovetich N.J., Krauss S., Webby R.J., Webster R.G. (2010). Puzzling inefficiency of H5N1 influenza vaccines in Egyptian poultry. PNAS, 107: 11044–11049.10.1073/pnas.1006419107Search in Google Scholar

Koch G., Steensels M., vanden Berg T. (2009). Vaccination of birds other than chickens and turkeys against avian influenza. Rev. Sci. Techniq., 28: 307–318.10.20506/rst.28.1.1872Search in Google Scholar

Landy N., Ghalamkari G., Toghyani M. (2011 a). Performance, carcass characteristics and immunity in broiler chicks fed dietary Neem (Azadirachta indica) as alternative for an antibiotic growth promoter. Livest. Sci., doi:10.1016/j.livsci.2011.08.017.10.1016/j.livsci.2011.08.017Open DOISearch in Google Scholar

Landy N., Ghalamkari G., Toghyani M., Moattar F. (2011 b). The effects of Echinacea purpurea L. (purple coneflower) as an antibiotic growth promoter substitution on performance, carcass characteristics and humoral immune response in broiler chickens. J. Med. Plants Res., 5: 2332e8.Search in Google Scholar

Lecu A., De Langhe C., Petit T., Bernard F., Swam H. (2009). Serologic response and safety to vaccination against avian influenza using inactivated H5N2 vaccine in zoo birds. J. Zoo Wildlife Med., 40: 731–743.10.1638/2008-0044.1Search in Google Scholar

Lee C.W., Senne D.A., Suarez D.L. (2004). Effect of vaccine use in the evolution of mexican lineage H5N2 avian influenza virus. J. Virol., 78: 8372–8381.10.1128/JVI.78.15.8372-8381.2004Search in Google Scholar

Lee D.H., Song C.S. (2013). H9N2 avian influenza virus in Korea: evolution and vaccination. Clin. Exp. Vac. Res., 2: 26–33.10.7774/cevr.2013.2.1.26Search in Google Scholar

Lee H.Y., Lee Y.N., Youn H.N., Lee D., Kwak J.H., Seong B., Lee J.B., Park S.Y., Choi I.S., Song C.S. (2012). Anti-influenza virus activity of green tea by-products in vitro and efficacy against influenza virus infection in chickens. Poultry Sci., 91: 66–73.10.3382/ps.2011-01645Search in Google Scholar

Li J., Zhong Y., Li H., Zhang N., Ma W., Cheng G., Liu F., Liu F., Xu J. (2011). Enhancement of astragalus polysaccharide on the immune responses in pigs inoculated with foot-and mouth disease virus vaccine. Int. J. Biol. Macromol., 49: 362–368.10.1016/j.ijbiomac.2011.05.015Search in Google Scholar

Li L.J., Ming Y.L., Li Y.T., Feng J.J., Hao F.Q., Zhang L. (2012). Adjuvant activity of Sargassum pallidum polysaccharides against combined Newcastle disease, infectious bronchitis and avian influenza inactivated vaccines. Marine Drugs, 10: 2648–2660.10.3390/md10122648Search in Google Scholar

Liu J., Chen H.B., Zhao Z.Z., Wang B., Zhao Y.Y., Yi T. (2009). Quality evaluation of Radix astragali from different sources in China. J. Chinese Pharmac. Sci., 18: 14–19.Search in Google Scholar

Maas R., Rosema S., van Zoelen D., Venema S. (2011). Maternal immunity against avian influenza H5N1 in chickens: limited protection and interference with vaccine efficacy. Avian Pathol., 40: 87–92.10.1080/03079457.2010.541226Search in Google Scholar

Mady W., Arafa A., Hussein A.S., Aly M.M., Madbouly H. (2013). Nigella sativa oil as an immunostimulant adjuvant in H5 based DNA vaccine of H5N1 avian influenza virus. Global Vet., 10: 663–668.Search in Google Scholar

Mahmood M.S., Amir H.W., Abbas R.Z., Rafique A., Aslam B. (2018). Evaluation of antiviral activity of Azadirachta indica (neem) bark extract against Newcastle disease virus. Pakistan Vet. J., 38: 25–28.10.29261/pakvetj/2018.005Search in Google Scholar

Mahmoodi M.B., Ghazanfari S., Salehi A., Sharifi S.D. (2014). Growth performance, carcass characteristics, antibody titers and blood parameters in broiler chickens fed dietary myrtle (Myrtus communis) essential oil as an alternative to antibiotic growth promoter. Poultry Sci., 2: 37–49.Search in Google Scholar

Miran S.N.K., Torshizi M.A.K., Bassami M.R., Jandaghi H. (2010). Effect of three immunostimulants on some of indicators of broilers’ immune response. Poultry Sci., 47: 321–325.10.2141/jpsa.009114Search in Google Scholar

Najafzadeh H., Ghorbanpour M., Mayahi M., Gavzan H. (2011). Effect of Echinacea purpurea on antibody production against fowl influenza vaccine. J. Appl. Anim. Res., 39: 139–141.10.1080/09712119.2011.565555Search in Google Scholar

Nanekarani S., Goodarzi M., Heidari M. (2012). The effect of different levels of spearmint (Mentha spicata) extract on immune system and blood parameters of broiler chickens. Apcbee Procedia, 4: 135–139.10.1016/j.apcbee.2012.11.023Search in Google Scholar

Nouzarian R., Tabeidian S., Toghyani M., Ghalamkari G. (2011). Effect of turmeric powder on performance, carcass traits, humoral immune responses, and serum metabolites in broiler chickens. J. Anim. Feed Sci., 20: 389–400.10.22358/jafs/66194/2011Search in Google Scholar

Oh S., Martelli P., Hock O.S., Luz S., Furley C., Chiek E.J., Wee L.C., Keun N.M. (2005). Field study on the use of inactivated H5N2 vaccine in avian species. Vet. Record, 157: 299–300.10.1136/vr.157.10.299Search in Google Scholar

OIE – Office International des Epizooties. World Organization for Animal Health (2012). Outbreaks of highly pathogenic avian influenza. Available from: http://www.oie.int/fileadmin/Home/eng/Animal_Health_in_the_World/docs/pdf/-graph_avian_influenza/graphs_HPAI_11_03_2012.pdfSearch in Google Scholar

Oyuntsetseg N., Khasnatinov M.A., Molor-Erdene P., Oyunbileg J., Liapunov A.V., Danchinova G.A., Oldokh S., Baigalmaa J., Chimedragchaa C. (2014). Evaluation of direct antiviral activity of the Deva-5 herb formulation and extracts of five Asian plants against influenza A virus H3N8 BMC. Compl. Alternat. Med., 14: 235.10.1186/1472-6882-14-235Search in Google Scholar

Paludan S.R. (2001). Requirements for the induction of interleukin-6 by herpes simplex virus-infected leukocytes. J. Virol., 75: 8008–8015.10.1128/JVI.75.17.8008-8015.2001Search in Google Scholar

Pantin-Jackwood M.J., Swayne D.E. (2009). Pathogenesis and pathobiology of avian influenza virus infection in birds. Rev. Sci. Tech., 28: 113–136.10.20506/rst.28.1.1869Search in Google Scholar

Park K.J., Kwon H.I., Song M.S., Pascua P.N., Baek Y.H., Lee J.H., Jang H.L., Lim J.Y., Mo I.P., Moon H.J., Kim C.J., Choi Y.K. (2011). Rapid evolution of low-pathogenic H9N2 avian influenza viruses following poultry vaccination programmes. J. Gener. Virol., 92: 36–50.10.1099/vir.0.024992-0Search in Google Scholar

Philippa J.D., Munster V.J., Bolhuis H., Bestebroer T.M., Schaftenaar W., Beyer W.E., Fouchier R.A., Kuiken T., Osterhaus A.D. (2005). Highly pathogenic avian influenza (H7N7): vaccination of zoo birds and transmission to non-poultry species. Vaccine, 23: 5743–5750.10.1016/j.vaccine.2005.09.013Search in Google Scholar

Qureshi A.S., Rehan S., Enbergs H. (2017). Nigella sativa seed extract affects granulocyte phagocytosis and lymphocytes proliferation in goats. Pakistan Vet. J., 37: 411–414.Search in Google Scholar

Rajput N., Naeem M., Ali S., Zhang J.F., Zhang L., Wang T. (2013). The effect of dietary supplementation with the natural carotenoids curcumin and lutein on broiler pigmentation and immunity. J. Poultry Sci., 92: 1177–1185.10.3382/ps.2012-02853Search in Google Scholar

Rajput Z.I., Xiao C., Hu S., Arijo A.G., Soomro N.M. (2007). Improvement of the efficacy of influenza vaccination (H5N1) in chicken by using extract of Cochinchina momordica seed (ECMS). J. Zhejiang Univ. Sci., 8: 331–337.10.1631/jzus.2007.B0331Search in Google Scholar

Rodrigo N., Martins da S. (2012). An overview on avian influenza. Braz. J. Poultry Sci., 14: 2.10.1590/S1516-635X2012000200001Search in Google Scholar

Rostami H., Seidavi A., Dadashbeiki M., Asadpour Y., Simões J., Assar A.S., Laudadio V., Losacco C., Perillo A., Tufarelli V. (2018). Supplementing dietary rosemary (Rosmarinus officinalis L.) powder and vitamin E in broiler chickens: evaluation of humoral immune response, lymphoid organs, and blood proteins. Environ. Sci. Pollut. Res. Int., 25: 8836–8842.10.1007/s11356-018-1209-xSearch in Google Scholar

Saif M. (2015). Olive leaf extract (OLE) exhibits antiviral activity against H5N1 avian influenza virus. ResearchGate, doi: 10.13140/2.1.5122.1286.Search in Google Scholar

Saki A.A., Kalantar M., Khoramabadi V. (2014). Effects of drinking thyme essence (Thymus vulgaris L.) on growth performance, immune response and intestinal selected bacterial population in broiler chickens. Poultry Sci. J., 2: 113–123.Search in Google Scholar

Sarfati-Mizrahi D., Lozano-Dubernard B., Soto-Priante E., Castro-Peralta F., Flores-Castro R., Loza-Rubio E., Gay-Gutiérrez M. (2010). Protective dose of a recombinant Newcastle disease LaSota-avian influenza virus H5 vaccine against H5N2 highly pathogenic avian influenza virus and velogenic viscerotropic Newcastle disease virus in broilers with high maternal antibody levels. Avian Dis., 54: 239–241.10.1637/8735-032509-Reg.1Search in Google Scholar

Sasmito E., Harimurti S., Nurhidayat H., Anggoro W., Hikmawati E.N., Wibowo J.T., Evi A.S., Hilmi N. (2012). Influence of Morinda citrifolia L. fruit extract as adjuvant on IgY production raised in laying chickens against avian influenza vaccine. Indonesian J. Pharmacol., 23: 115–120.Search in Google Scholar

Setiyono A., Bermawiedan N. (2014). Histopathological and clinical studies on herbal chicken after challenging with avian influenza H5N1 virus. J. Kedokteran Hewan, 8: 1.10.21157/j.ked.hewan.v8i1.1252Search in Google Scholar

Shah M.U., Aslam A., Mustafa G., Zahid B., Imran M.S. (2018). Effect of mentofin and asimirus on humoral immune response and tissue changes in infectious bursal disease vaccinated broiler birds. Pakistan Vet. J., 38: 56–60.10.29261/pakvetj/2018.011Search in Google Scholar

Shang R., Liang J., Na Z., Yang H., Lu Y., Hua L., Guo W., Cui Y., Wang L. (2010). In vivo inhibition of NAS preparation on H9N2 subtype AIV. Virol. Sin., 25: 145–150.10.1007/s12250-010-3082-8Search in Google Scholar

Shokraneh M., Ghalamkari G., Toghyani M., Landy N. (2016). Influence of drinking water containing Aloe vera (Aloe barbadensis Miller) gel on growth performance, intestinal microflora, and humoral immune responses of broilers. Vet. World, 9: 1197–1203.10.14202/vetworld.2016.1197-1203Search in Google Scholar

Suarez D.L. (2005). Overview of avian influenza DIVA test strategies. Biologicals, 33: 221–226.10.1016/j.biologicals.2005.08.003Search in Google Scholar

Suarez D., Schultz-Cherry S. (2000). Immunology of avian influenza virus: a review. Develop. Comp. Immunol., 24: 269–283.10.1016/S0145-305X(99)00078-6Search in Google Scholar

Subhani Z., Shahid M., Hussain F., Khan J.A. (2018). Efficacy of Chlorella pyrenoidosa to ameliorate the hepatotoxic effects of aflatoxin B1 in broiler chickens. Pakistan Vet. J., 38: 13–18.10.29261/pakvetj/2018.003Search in Google Scholar

Sun N., Sun P., Xie N., Khan A., Sun Y., Fan K., Yin W., Li H. (2018). Antiviral and immunomodulatory effects of dipotassium glycyrrhizinate in chicks artificially infected with infectious bursal disease virus. Pakistan Vet. J., 39: 43–48.10.29261/pakvetj/2018.109Search in Google Scholar

Sun R., Luo J., Gao Y., He H. (2009). Different infection routes of avian influenza A (H5N1) virus in mice. Integ. Zool., 4: 402–408.10.1111/j.1749-4877.2009.00178.xSearch in Google Scholar

Taheri H.R., Rahmani H.R., Pourreza J. (2005). Humoral immunity of broilers is affected by oil extracted propolis (OEP) in the diet. Int. J. Poultry Sci., 4: 414–417.10.3923/ijps.2005.414.417Search in Google Scholar

Talazadeh F., Mayahi M., Varzi H.N., Norouzizade H. (2015). Effect of Thymus vulgaris extract on systemic antibody responses against influenza and Newcastle disease vaccine in broiler chickens. J. Herbal Drugs, 6: 41–46.Search in Google Scholar

Talazadeh F., Mansoor M., Marziye N. (2016). The effect of Antibiofin^® on the immune response against avian influenza subtype H9N2 vaccine in broiler chickens. Int. J. Enteric Pathol., 4: e39396.10.15171/ijep.2016.04Search in Google Scholar

Tian G., Zhang S., Li Y., Bu Z., Liu P., Zhou J., Li C., Shi J., Yu K., Chen H. (2005). Protective efficacy in chickens, geese and ducks of an H5N1-inactivated vaccine developed by reverse genetics. Virology, 341: 153–162.10.1016/j.virol.2005.07.011Search in Google Scholar

Toghyani M., Faghan N. (2017). Effect of sumac (Rhus coriaria L.) fruit powder as an antibiotic growth promoter substitution on growth performance, immune responses and serum lipid profile of broiler chicks. Indian J. Pharmac. Educ. Res., 51: 295–298.10.5530/ijper.51.3s.33Search in Google Scholar

Toghyani M., Tohidi M., Gheisari A.A., Tabeidian S.A. (2010). Performance, immunity, serum biochemical and hematological parameters in broiler chicks fed dietary thyme as alternative for an antibiotic growth promoter. Afr. J. Biotechnol., 9: 6819–6825.Search in Google Scholar

Toghyani M., Toghyani M., Gheisari A., Ghalamkari G., Eghbalsaied S. (2011). Evaluation of cinnamon and garlic as antibiotic growth promoter substitutions on performance, immune responses, serum biochemical and haematological parameters in broiler chicks. Livest. Sci., 138: 167–173.10.1016/j.livsci.2010.12.018Search in Google Scholar

Toghyani M., Tohidi M., Gheisari A., Tabeidian A., Toghyani M. (2012). Evaluation of oyster mushroom as a biological growth promoter on performance, humoral immunity and blood characteristics of broiler chicks. Poultry Sci., 49: 183–190.10.2141/jpsa.011068Search in Google Scholar

Toghyani M., Mosavi S., Modaresi M., Landy N. (2015). Evaluation of kefir as a potential probiotic on growth performance, serum biochemistry and immune responses in broiler chicks. Anim. Nutr., 1: 305–309.10.1016/j.aninu.2015.11.010Search in Google Scholar

Tohid T., Hasan G., Alireza T. (2010). Efficacy of mannanoligosaccharides and humate on immune response to avian influenza (H9) disease vaccination in broiler chickens. Vet. Res. Commun., 34: 709–717.10.1007/s11259-010-9444-8Search in Google Scholar

Trinchieri G. (2003). Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol., 3: 133–146.10.1038/nri1001Search in Google Scholar

Umar S., Rehman A., Younus M., un-Nisa Q., Ali A., Shahzad M., Ali A.M., Munir M.T., Bin Aslam H., Yaqoob M. (2015). Effects of Nigella sativa on immune responses and pathogenesis of avian influenza (H9N2) virus in turkeys. J. Appl. Poultry Res., 25: 95–103.10.3382/japr/pfv070Search in Google Scholar

Umar S., Tanveerunir M., Subhan S., Azam T., un Nisa Q., Irfan Khan M., Umar W., ur Rehman Z., Sattar Saqib A., Ali Shah M. (2016 a). Protective and antiviral activities of Nigella sativa against avian influenza (H9N2) in turkeys. J. Saudi Soc. Agr. Sci., doi: http://dx.doi.org/10.1016/j.jssas.2016.09.00410.1016/j.jssas.2016.09.004Open DOISearch in Google Scholar

Umar S., Shah M.A.A., Munir M.T., Yaqoob M., Fiaz M., Anjum S., Kaboudi K., Bouzouaia M., Younus M., Nisa Q., Iqbal M., Umar W. (2016 b). Synergistic effects of thymoquinone and curcumin on immune response and anti-viral activity against avian influenza virus (H9N2) in turkeys. Poultry Sci., 95: 1513–1520.10.3382/ps/pew06926944958Search in Google Scholar

Velazquez-Salinas L., Verdugo-Rodriguez A., Rodriguez L.L., Borca M.V. (2019). The role of interleukin 6 during viral infections. Front. Microbiol., 10: 1057.10.3389/fmicb.2019.01057Search in Google Scholar

Vetter J., Lelley J. (2004). Selenium level of the cultivated mushroom Agaricus bisporus. Acta Aliment., 33: 297–301.10.1556/AAlim.33.2004.3.10Search in Google Scholar

Widhowati D., Hidayah N., Yunani R., Malia M. (2018). Early study the potency of turmeric (Curcuma domestica val.) as immunostimulator for layers chickens against avian influenza (AI) vaccine. Adv. Soc. Sci., Educ. Human. Res., Doi: 10.2991/icpsuas-17.2018.62.10.2991/icpsuas-17.2018.62Open DOISearch in Google Scholar

Willis W.L., Isikhuemhen O.S., Ibrahim S.A. (2007). Performance assessment of broiler chickens given mushroom extract alone or in combination with probiotics. Poultry Sci., 6: 1856–1860.10.1093/ps/86.9.1856Search in Google Scholar

Xie Q., Li X., Sanpha K., Ji J., Xi Q., Xue C., Ma J., Zhang Y. (2012). Pinon shell polysaccharide enhances immunity against H9N2 avian influenza virus in chickens. Poultry Sci., 91: 2767–2773.10.3382/ps.2012-02431Search in Google Scholar

Yang Y., Feng W.S. (1998). Brochures of isolation and extraction of chemical components from herbs (in Chinese). Chin. Herbal Med. Press, Beijing.Search in Google Scholar

Yazdi F.F., Ghalamkari G., Toghyani M., Modaresi M., Landy N. (2014). Efficiency of Tribulus terrestris L. as an antibiotic growth promoter substitute on performance and immune responses in broiler chicks. Asian Pac. J. Trop. Dis., 4: 1014–1018.10.1016/S2222-1808(14)60774-XSearch in Google Scholar

Yu J., Shi F.S., Hu S. (2015). Improved immune responses to a bivalent vaccine of Newcastle disease and avian influenza in chickens by ginseng stem-leaf saponins. Vet. Immunol. Immunopathol., 167: 147–155.10.1016/j.vetimm.2015.07.017Search in Google Scholar

Yuniwarti Y.W.E., Asmara W., Artama W., Tabbu R.C. (2012). The effect of virgin coconut oil on lymphocyte and cd4 in chicken vaccinated against Avian Influenza Virus. J. Indonesian Tropic. Anim. Agric., 37: 64–69.10.14710/jitaa.37.1.64-69Search in Google Scholar

Yuniwarti Y.W.E., Widya A., Artama W., Rangga T.C. (2015). Virgin coconut oil supplementation increased the survival of avian influenza virus (H5N1) infected chicken. Asian J. Poultry Sci., 9: 106–111.10.3923/ajpsaj.2015.106.111Search in Google Scholar

Zhai L., Li Y., Wang W., Hu S. (2011). Enhancement of humoral immune responses to inactivated Newcastle disease and avian influenza vaccines by oral administration of ginseng stem-and-leaf saponins in chickens. Poultry Sci., 90: 1955–1959.10.3382/ps.2011-01433Search in Google Scholar

Zohreh P., Qotbi A., Seidavi A., Laudadio V., Centoducati G., Vincenzo T. (2014). Effect of different levels of dietary sweet orange (Citrus sinensis) peel extract on humoral immune system responses in broiler chickens. Anim. Sci. J., 86: 105–110.10.1111/asj.12250Search in Google Scholar