Petrusha YuK, Silin DA, Lebedev SV.

Animal Husbandry and Fodder Production. 2025. Vol. 108. No. 1. Р. 33-49.

doi:10.33284/2658-3135-108-1-33

 

Review article

Factors and modulators of the avian immune system

 

Yuri K Petrusha1, Dmitriy A Silin2, Svyatoslav V Lebedev3

1,2,3Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences, Orenburg, Russia

1shadow752@yandex.ru, https://orcid.org/0000-0002-8283-2972

2dasilin@mail.ru, https://orcid.org/0000-0001-6438-139X

3lsv74@list.ru, https://orcid.org/0000-0001-9485-7010

 

Abstract. The modern development of poultry breeding is marked by genetic and breeding achievements aimed at increasing productivity and reducing rearing time. Prospects of modern research are directed to the search for new technologies that contribute to the increase of organism resistance and reveal genetic potential. The presented review systematizes data on structural and functional features of the immune system of poultry, considers etiological factors of immunosuppression and analyzes determinants affecting the formation of nonspecific resistance of the organism. The data on the key role of essential trace elements, including zinc, selenium, iron, iodine, manganese and copper, in the regulation of immune status are presented.

Keywords: hens, layers, broilers, immune system, immune response, microelements, productivity

Acknowledgments:  the  work   was   supported  by  the  Russian  Science  Foundation,  Project  No. 22-16-00070.

For citation:  Petrusha YuK, Silin DA, Lebedev SV. Factors and modulators of the avian immune system (review). Animal Husbandry and Fodder Production. 2025;108(1):33-49. (In Russ.). doi: https://doi.org/10.33284/2658-3135-108-1-33

References

 

  1. Fisinin VI, Egorova TA, Egorov IA. The effects of diets with reduced levels of energy, lysine, and methionine and different dietary forms of these amino acids on non-specific immunity, natural resistibility, and nutrient digestibility in broiler breeder hens. Poultry Farming. 2022;10:58-63.
  2. Kurilkina MY, Kholodilina TN, Muslyumova DM. Effect of highly dispersed metals on morphological and biochemical characteristics of broiler chickens’ blood. Animal Husbandry and Fodder Production. 2018;101(3):93-99.
  3. Lebedev SV, Gubaidullina IZ, Vershinina IA et al. The effect of chromium-containing ultrafine particles on the morphofunctional characteristics of organism of broiler chickens. Animal Husbandry and Fodder Production. 2019;102(4):23-32. doi: 10.33284/2658-3135-102-4-23
  4. Molokanova OV. Vitamins and trace elements in poultry nutrition: the importance of a rational approach. Poultry Farming. 2024;73(12):31-36. doi: 10.33845/0033-3239-2024-73-12-31-36
  5. Sizova ЕА, Korolev VL, Makaev ShA, Miroshnikova EP, Shakhov VA. Morphological and biochemical blood parameters in broilers at correction with dietary copper salts and nanoparticles. Sel’skokhozyaistvennaya biologiya [Agricultural Biology]. 2016;51(6):903-911. doi: 10.15389/agrobiology.2016.6.903eng
  6. Nechitailo KS, Sizova EA. Evaluation of influence of ultrafine particles of copper and a complex enzymatic additive on productive performance of broiler chickens. Animal Husbandry and Fodder Production. 2022;105(4):8-20. doi: 10.33284/2658-3135-105-4-8
  7. Nechitaylo KS, Sizova EA, Ryazantseva KV. Changes in the elemental status of the organism when administered a feed additive based on enzymes in complex with ultradisperse copper. Trace Elements in Medicine. 2024;25(2):74-76. doi: 10.19112/2413-6174-2024-25-2-33
  8. Egorov I, Andrianova E, Grigor'eva E, et al. Organic form of copper in mixed fodder for broiler chickens. Compound feeds. 2020;4:37-41. doi: 10.25741/2413-287X-2020-04-3-099
  9. Suraj PF, Fisinin VI, Kochish II. From regulation of vitagens to optimization of immune response: new approaches to immunomodulation in poultry farming. Proceedings of XX international conference "Poultry production in Russia and in the world: present state, dynamics of development, prospective innovations" (Sergiev Posad, 08 - 10 October 2020). Sergiev Posad: All-Russian Research and Technological Institute of Poultry Farming; 2020:56-66.
  10. Sizova EA, Nechitailo KS, Ivanischeva AP, Ryabov NI. The prospects of using ultra-dispersed forms of metals in animal feeding. Animal Husbandry and Fodder Production. 2020;103(3):177-189. doi: 10.33284/2658-3135-103-3-177
  11. Sizova EA, Miroshnikov SA, Nechitailo KS. The effectiveness of various forms of zn as stimulators of the immune response in broiler chickens (Gallus Gallus). Sel’skokhozyaistvennaya biologiya [Agricultural Biology]. 2023;58(2):373-385. doi: 10.15389/agrobiology.2023.2.373eng
  12. Frolov AN, Nechitailo KS, Kosinova MS. Influence of various forms of copper and zinc on the elemental status of broiler chickens. (Conference proceedings) Nanotechnologies in agriculture: prospects and  risks:  materials  of  the  international  scientific and practical conference, (Orenburg, 26-27 September 2018). Orenburg: FRC BST RAS; 2018:158-162.
  13. Abdel-Shafi S, Abd El-Hack  ME,  Amen S, Helmi A, Swelum AA, Tellez-Isaias G, Enan G. The efficacy of some probiotics and prebiotics on the prevalence of E. coli and the immune response of chickens. Poult Sci. 2023;102(12):103219. doi: 10.1016/j.psj.2023.103219
  14. Abo-Al-Ela HG, El-Kassas S, El-Naggar K, Abdo SE, Jahejo AR, Al Wakeel RA. Stress and immunity in poultry: light management and nanotechnology as effective immune enhancers to fight stress. Cell Stress and Chaperones. 2021;26(3):457-472. https://doi.org/10.1007/s12192-021-01204-6
  15. Adekunle LA, Ola OO, Adesola RO, Adekunle UA, Taiwo OV, Jubril AJ, Arthur JF. The effect of micronutrient supplementation on bioavailability, antioxidants activity, and weight gain in response to Infectious Bursal Disease vaccination in commercial broilers. Vet Anim Sci. 2023;21:100309. doi: 10.1016/j.vas.2023.100309
  16. AL-Ruwad SH, Attia AI,  Abdel Monem  UM, Abdel-Maksoud A, Thagfan FA, Alqahtani HA, Alkahtani AM, Salah AS, Reda FM. Dietary supplementation with copper nanoparticles enhances broiler performance by improving growth, immunity, digestive enzymes, and gut microbiota. Poultry Science. 2024;103(10):104026. https://doi.org/10.1016/j.psj.2024.104026
  17. Amevor FK, Cui Z, Ning Z, Du X, Jin N, Shu G, Deng X, Zhu Q, Tian Y, Li D, Wang Y, Zhang Z, Zhao X. Synergistic effects of quercetin and vitamin E on egg production, egg quality, and immunity in aging breeder hens. Poult Sci. 2021;100(12):101481. doi: 10.1016/j.psj.2021.101481
  18. Aminullah N, Prabhu TM, Naik J, Suresh BN, Indresh HC. Performance of Swarnadhara breeder hens supplemented with reduced levels of different copper forms. Vet World. 2021;14(5):1371-1379. doi: 10.14202/vetworld.2021.1371-1379
  19. Davison S, Tracy L,  Kelly DJ, Bender SJ, Pierdon MK, Mills J, Barnhart DJ, Licciardello S, Anis EAM, Wallner-Pendleton E, Dunn P, Robinson C, Ladman B, Kuchipudi SV. Infectious coryza in Pennsylvania. Avian Dis. 2024;68(3):175-182. doi: 10.1637/aviandiseases-D-23-00073
  20. De Luca C, Schachner A, Mitra T, Heidl S, Liebhart D, Hess M. Fowl adenovirus (FAdV) fiber-based vaccine  against  inclusion  body  hepatitis  (IBH)  provides  type-specific  protection  guided by  humoral  immunity  and  regulation  of  B  and  T  cell response. Vet Res. 2020;51(1):143. doi: 10.1186/s13567-020-00869-8
  21. Deng Z, Han D, Wang Y, Wang Q, Yan X, Wang S, Liu X, Song W, Ma Y. Lactobacillus casei protects intestinal mucosa from damage in chicks caused by Salmonella pullorum via regulating immunity and the Wnt signaling pathway and maintaining the abundance of gut microbiota. Poult Sci. 2021;100(8):101283. doi: 10.1016/j.psj.2021.101283
  22. Forouzandeh A, Blavi L, Abdelli N, Melo-Duran D, Vidal A, Rodríguez M, Monteiro ANTR, Pérez JF, Darwich L, Solà-Oriol D. Effects of dicopper oxide and copper sulfate on growth performance and gut microbiota in broilers. Poultry Science. 2021;100(8):101224. https://doi.org/10.1016/j.psj.2021.101224
  23. Goel A. Heat stress management in poultry. J Anim Physiol Anim Nutr (Berl). 2021;105(6):1136-1145. doi: 10.1111/jpn.13496
  24. Habibian M, Ghazi S, Moeini MM, Abdolmohammadi A. Effects of dietary selenium and vitamin E on immune response and biological blood parameters of broilers reared under thermoneutral or heat stress conditions. Int J Biometeorol. 2014;58(5):741-752. doi: 10.1007/s00484-013-0654-y
  25. Hafez HM, Attia YA. Challenges to the poultry industry: current perspectives and strategic future after the COVID-19 outbreak. Front Vet Sci. 2020;7:516. doi: 10.3389/fvets.2020.00516
  26. Hemida MG, Al-Hammadi M, Gonzalves C, Ismail MM. The experimental infection with a field isolate of the infectious bronchitis virus from eastern Saudi Arabia resulted in seroconversion of the challenged birds with no apparent clinical diseases. Virusdisease. 2021;32(2):354-360. doi: 10.1007/s13337-021-00675-6
  27. Hidayat C,  Sumiati S,  Jayanegara  A,  Wina E. Effect of zinc addition on the immune response and production performance of broilers: a meta-analysis. Asian-Australasian  Journal  of  Animal Sciences. 2020;33(3): 465-479. https://doi.org/10.5713/ajas.19.0146
  28. Hofmann T, Schmucker SS, Bessei W, Grashorn M, Stefanski V. Impact of housing environment on the immune system in chickens: a review. Animals (Basel). 2020;10(7):1138. doi: 10.3390/ani10071138
  29. Hu Q, Zhang T, He H, Pu F, Zhang R, Li L, Hu J, Bai L, Han C, Wang J, Liu H. Impacts of longitudinal water curtain cooling system on transcriptome-related immunity in ducks. BMC Genomics. 2024;25(1):333. doi: 10.1186/s12864-024-10179-4
  30. Jett KA, Baker ZN,  Hossain A,  Boulet A, Cobine PA, Ghosh S, Ng P, Yilmaz O, Barreto K,  DeCoteau J, Mochoruk K, Ioannou GN, Savard C, Yuan S, Abdalla OH, Lowden C, Kim BE, Cheng HM, Battersby BJ, Gohil VM, Leary SC. Mitochondrial dysfunction reactivates α-fetoprotein expression that drives copper-dependent immunosuppression in mitochondrial disease models. J Clin Invest. 2023;133(1):e154684. doi: 10.1172/JCI154684
  31. Kulappu Arachchige  SN,  Kanci Condello A, Zhu L, Shil PK, Tivendale KA, Underwood GJ, Noormohammadi AH, Browning GF, Wawegama NK. Effects of immunosuppression on the efficacy of vaccination against Mycoplasma gallisepticum infection in chickens. Vet Microbiol. 2021;260:109182. doi: 10.1016/j.vetmic.2021.109182
  32. Lan D, Xun X, Hu Y, Li N, Yang C, Jiang X, Liu Y. Research on the effect of Pediococcus pentosaceus on Salmonella enteritidis-infected chicken. Biomed Res Int. 2020;2020:6416451. doi: 10.1155/2020/6416451
  33. Lebedev S, Kazakova T, Marshinskaia O. Influence of feed supplementation with probiotic and organic form of zinc on functional status of broiler chickens. Open Vet J. 2024;14(9):2181-2191. doi: 10.5455/OVJ.2024.v14.i9.7
  34. Lee M, Hosseindoust A, Oh S, Ko H, Cho E, Sa S, Kim Y, Choi J, Kim J. Impact of an anti-Salmonella. Typhimurium bacteriophage on intestinal microbiota and immunity status of laying hens. J Anim Physiol Anim Nutr (Berl). 2021;105(5):952-959. doi: 10.1111/jpn.13424
  35. Lin X, Gou Z, Wang Y, Li L, Fan Q, Ding F, Zheng C, Jiang S. Effects of dietary iron level on growth performance, immune organ indices and meat quality in chinese yellow broilers. Animals (Basel). 2020;10(4):670. doi: 10.3390/ani10040670
  36. Liu Q, Yang J, Huang X, Liu Y, Han K, Zhao D, Zhang L, Li Y. Transcriptomic profile of chicken bone marrow-derive dendritic cells in response to H9N2 avian influenza A virus. Vet Immunol Immunopathol. 2020;220:109992. doi: 10.1016/j.vetimm.2019.109992
  37. Méndez AAE, Mendoza JI, Echarren ML, Terán I, Checa SK, Soncini FC. Evolution of copper homeostasis and virulence in salmonella. Front Microbiol. 2022;13:823176. doi: 10.3389/fmicb.2022.823176
  38. Mohamed RI, Elsamadony HA, Alghamdi RA, Eldin ALAZ, El-Shemy A, Abdel-Moez Amer S, Bahshwan SMA, El-Saadony MT, El-Sayed HS, El-Tarabily KA, Saad ASA. Molecular and pathological screening of the current circulation of fowlpox and pigeon pox virus in backyard birds. Poult Sci. 2024;103(12):104249. doi: 10.1016/j.psj.2024.104249
  39. Morsy EA, Hussien AM, Ibrahim MA, Farroh KY, Hassanen EI. Cytotoxicity and genotoxicity of copper oxide nanoparticles in chickens. Biol Trace Elem Res. 2021;199(12):4731-4745. doi: 10.1007/s12011-021-02595-4
  40. Mroczek-Sosnowska N, Łukasiewicz M, Wnuk A, Sawosz E, Niemiec J, Skot A, Jaworski S, Chwalibog A. In ovo administration of copper nanoparticles and copper sulfate positively influences chicken performance: J Sci Food Agric. 2016;96(9):3058-3062. doi: 10.1002/jsfa.7477
  41. Nys Y, Schlegel P, Durosoy S, Jondreville C, Narcy A. Adapting trace mineral nutrition of birds for optimizing the environment and poultry product quality. World’s Poult Sci J. 2018;74(02):225-238. doi: 10.1017/S0043933918000016
  42. Ognik K, Stępniowska A, Cholewińska E, Kozłowski K. The effect of administration of copper nanoparticles to chickens in drinking water on estimated intestinal absorption of iron, zinc, and calcium. Poult Sci. 2016;95(9):2045-2051. doi: 10.3382/ps/pew200
  43. Panossian AG, Efferth T, Shikov AN, Pozharitskaya ON, Kuchta K, Mukherjee PK, Banerjee S, Heinrich M, Wu W, Guo DA, Wagner H. Evolution of the adaptogenic concept from traditional use to medical systems: Pharmacology of stress- and aging-related diseases. Med Res Rev. 2021;41(1):630-703. doi: 10.1002/med.21743
  44. Petruzzelli R, Polishchuk RS. Activity and trafficking of copper-transporting ATPases in tumor development and defense against platinum-based drugs. Cells. 2019;8(9):1080. doi: 10.3390/cells8091080
  45. Phillips CJC, Hosseintabar-Ghasemabad B, Gorlov IF, Slozhenkina MI, Mosolov AA, Seidavi A. Immunomodulatory effects of natural feed additives for meat chickens. Life (Basel). 2023;13(6):1287. doi: 10.3390/life13061287
  46. Ravikumar R, Chan J, Prabakaran M. Vaccines against major poultry viral diseases: strategies to improve the breadth and protective efficacy. Viruses. 2022;14(6):1195. doi: 10.3390/v14061195
  47. Sabaghi S, Razmyar J,  Heidarpour M. Effects of nano-manganese on humoral immune response and oxidative stress in broilers. Vet Res Forum. 2021;12(4):487-491. doi: 10.30466/vrf.2020.114233.2716
  48. Scott A, Vadalasetty KP, Chwalibog A, Sawosz E. Copper nanoparticles as an alternative feed additive in poultry diet: A review. Nanotechnol. Rev. 2018;7(1):69-93. doi: 10.1515/ntrev-2017-0159
  49. Sha Md Shahan Shahriar, Nazmul Haque, Tafsir Hasan, Md Tasif Amir Sufal, Mohammad Tariqul Hassan, Mahfujul Hasan, Sayed MA Salam, Heavy metal pollution in poultry feeds and broiler chickens in Bangladesh. Toxicology Reports. 2025;14:101932. https://doi.org/10.1016/j.toxrep.2025.101932
  50. Shirai T, Nakai A,  Ando  E,  Fujimoto  J, Leach S, Arimori T, Higo D, van Eerden FJ, Tulyeu J, Liu YC, Okuzaki D, Murayama MA, Miyata H, Nunomura K, Lin B, Tani A, Kumanogoh A, Ikawa M, Wing JB, Standley DM, Takagi J, Suzuki K. Celastrol suppresses humoral immune responses and autoimmunity by targeting the COMMD3/8 complex. Sci Immunol. 2023;8(81):eadc9324. doi: 10.1126/sciimmunol.adc9324
  51. Słupczyńska M, Jamroz D, Orda J, Wiliczkiewicz A, Kuropka P, Król B. The thyroid hormone and immunoglobulin concentrations in blood serum and thyroid gland morphology in young hens fed with different diets, sources, and levels of iodine supply. Animals. 2023;13(1):158. https://doi.org/10.3390/ani13010158
  52. Tian Y, Ma X, Jiang Y, Han J, Zhang R, Xu X, Zhang W, Man C. Circular RNA circAKIRIN2 participates in the process of stress-induced immunosuppression affecting immune response to infectious bursal disease virus vaccine in chicken. Vet Microbiol. 2023;281:109746. doi: 10.1016/j.vetmic.2023.109746
  53. Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, De Angelis M. The controversial role of human gut Lachnospiraceae. Microorganisms. 2020;8(4):573. doi: 10.3390/microorganisms8040573
  54. Weerts EAWS, Matthijs MGR, Bonhof J, van Haarlem DA, Dwars RM, Gröne A, Verheije MH, Jansen CA. The contribution of the immune response to enhanced colibacillosis upon preceding viral respiratory infection in broiler chicken in a dual infection model. Vet Immunol Immunopathol. 2021;238:110276. doi: 10.1016/j.vetimm.2021.110276
  55. Wlaźlak S, Pietrzak E, Biesek J, Dunislawska A. Modulation of the immune system of chickens a key factor in maintaining poultry production – a review. Poultry Science. 2023;102(8):102785. https://doi.org/10.1016/j.psj.2023.102785
  56. Yan HL, Cao SC, Hu YD, Zhang HF, Liu JB. Effects of methylsulfonylmethane on growth performance, immunity, antioxidant capacity, and meat quality in Pekin ducks. Poult Sci. 2020;99(2):1069-1074. doi: 10.1016/j.psj.2019.10.002
  57. Yang W, Liu X, Wang X. The immune system of chicken and its response to H9N2 avian influenza virus. Vet Q. 2023;43(1):1-14. doi: 10.1080/01652176.2023.2228360
  58. Ye X-Q, Zhu Y-R, Yang Y-Y, Qiu S-J, Liu W-C. Biogenic selenium nanoparticles synthesized with alginate oligosaccharides alleviate heat stress-induced oxidative damage to organs in broilers through activating Nrf2-mediated anti-oxidation and anti-ferroptosis pathways. Antioxidants 2023;12(11):1973. https://doi.org/10.3390/antiox12111973
  59. Zhen W, Zhu T, Wang P, Guo F, Zhang K, Zhang T, Jalukar S, Zhang Y, Bai D, Zhang C, Guo Y, Wang Z, Ma Y. Effect of dietary Saccharomyces-derived prebiotic refined functional carbohydrates as antibiotic alternative on growth performance and intestinal health of broiler chickens reared in a commercial farm. Poult Sci. 2023;102(6):102671. doi: 10.1016/j.psj.2023.102671

Information about the authors:

Yuri K Petrusha, Junior Researcher at the Laboratory of Precision Technologies in Agriculture, Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences, 29, 9 Yanvarya St., Orenburg, 460000, tel.: 89058877200.

Dmitriy A Silin, Junior Researcher at the Laboratory of Precision Technologies in Agriculture, Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences, 29, 9 Yanvarya St., Orenburg, 460000, tel.: 89534575189.

Svyatoslav V Lebedev, Dr. Sci. (Biology), Corresponding Member of the Russian Academy of Sciences, Leading Researcher of the Laboratory of Biological Tests and Examinations, Federal Research Centre of Biological Systems and Agrotechnologies of the Russian Academy of Sciences, 29, 9 Yanvarya St., Orenburg, 460000, tel.: 89123458738.

The article was submitted 13.11.2024; approved after reviewing 14.03.2025; accepted for publication 17.03.2025.

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