Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Management and control of coccidiosis in poultry - A review

  • Rafiq Ahmad (Department of Biotechnology and Animal Science, National Ilan University) ;
  • Yu-Hsiang Yu (Department of Biotechnology and Animal Science, National Ilan University) ;
  • Kuo-Feng Hua (Department of Biotechnology and Animal Science, National Ilan University) ;
  • Wei-Jung Chen (Department of Biotechnology and Animal Science, National Ilan University) ;
  • Daniel Zaborski (Department of Ruminants Science, West Pomeranian University of Technology) ;
  • Andrzej Dybus (Department of Genetics, West Pomeranian University of Technology) ;
  • Felix Shih-Hsiang Hsiao (Department of Biotechnology and Animal Science, National Ilan University) ;
  • Yeong-Hsiang Cheng (Department of Biotechnology and Animal Science, National Ilan University)
  • Received : 2023.05.17
  • Accepted : 2023.08.12
  • Published : 2024.01.01
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Abstract

Poultry coccidiosis is an intestinal infection caused by an intracellular parasitic protozoan of the genus Eimeria. Coccidia-induced gastrointestinal inflammation results in large economic losses, hence finding methods to decrease its prevalence is critical for industry participants and academic researchers. It has been demonstrated that coccidiosis can be effectively controlled and managed by employing anticoccidial chemical compounds. However, as a result of their extensive use, anticoccidial drug resistance in Eimeria species has raised concerns. Phytochemical/herbal medicines (Artemisia annua, Bidens pilosa, and garlic) seem to be a promising strategy for preventing coccidiosis, in accordance with the "anticoccidial chemical-free" standards. The impact of herbal supplements on poultry coccidiosis is based on the reduction of oocyst output by preventing the proliferation and growth of Eimeria species in chicken gastrointestinal tissues and lowering intestinal permeability via increased epithelial turnover. This review provides a thorough up-to-date assessment of the state of the art and technologies in the prevention and treatment of coccidiosis in chickens, including the most used phytochemical medications, their mode of action, and the applicable legal framework in the European Union.

Keywords

References

  1. Govoni C, Chiarelli DD, Luciano A, et al. Global assessment of natural resources for chicken production. Adv Water Resour 2021;154:103987. https://doi.org/10.1016/j.advwatres.2021.103987 
  2. Nkukwana T. Global poultry production: Current impact and future outlook on the South African poultry industry. S Afr J Anim Sci 2018;48:869-84. https://doi.org//10.4314/sajas.v48i5.7 
  3. Mesa-Pineda C, Navarro-Ruiz JL, Lopez-Osorio S, Chaparro-Gutierrez JJ, Gomez-Osorio LM. Chicken coccidiosis: from the parasite lifecycle to control of the disease. Front Vet Sci 2021;8:787653. https://doi.org/10.3389/fvets.2021.787653 
  4. Singh RB, Watson RR, Takahashi T. The role of functional food security in global health. Academic Press; 2019. pp. 3-24. https://doi.org/10.1016/B978-0-12-813148-0.00001-3
  5. Ahmad R, Yu YH, Hsiao FSH, et al. Influence of heat stress on poultry growth performance, intestinal inflammation, and immune function and potential mitigation by probiotics. Animals 2022;12:2297. https://doi.org/10.3390/ani12172297
  6. Aganovic K, Hertel C, Vogel RF, et al. Aspects of high hydrostatic pressure food processing: Perspectives on technology and food safety. Compr Rev Food Sci Food Saf 2021;20:3225-66. https://doi.org/10.1111/1541-4337.12763 
  7. Blake DP, Knox J, Dehaeck B, et al. Re-calculating the cost of coccidiosis in chickens. Vet Res 2020;51:115. https://doi.org/10.1186/s13567-020-00837-2 
  8. Lahlou RA, Bounechada M, Mohammedi A, Silva LR, Alves G. Dietary use of Rosmarinus officinalis and Thymus vulgaris as anticoccidial alternatives in poultry. Anim Feed Sci Technol 2021;273:114826. https://doi.org/10.1016/j.anifeedsci.2021.114826 
  9. Geng T, Ye C, Lei Z, et al. Prevalence of Eimeria parasites in the Hubei and Henan provinces of China. Parasitol Res 2021;120:655-63. https://doi.org/10.1007/s00436-020-07010-w
  10. Kers JG, Velkers FC, Fischer EA, Hermes GDA, Stegeman JA, Smidt H. Host and environmental factors affecting the intestinal microbiota in chickens. Front Microbiol 2018;9:235. https://doi.org/10.3389/fmicb.2018.00235
  11. Yang C, Kennes YM, Lepp D, et al. Effects of encapsulated cinnamaldehyde and citral on the performance and cecal microbiota of broilers vaccinated or not vaccinated against coccidiosis. Poult Sci 2020;99:936-48. https://doi.org/10.1016/j.psj.2019.10.036
  12. Hamid PH, Kristianingrum YP, Wardhana AH, Prastowo S, Silva LMR. Chicken coccidiosis in Central Java, Indonesia: A recent update. Vet Med Int 2018;2018:8515812. https://doi.org/10.1155/2018/8515812
  13. Martins RR, Silva LJ, Pereira AM, Esteves A, Duarte SC, Pena A. Coccidiostats and poultry: A comprehensive review and current legislation. Foods 2022;11:2738. https://doi.org/10.3390/foods11182738
  14. Nogueira VA, Franca TN, Peixoto PV. Ionophore poisoning in animals. Pesqui Vet Bras 2009;29:191-7. https://doi.org/10.1590/S0100-736X2009000300001
  15. El-Shall NA, Abd El-Hack ME, Albaqami NM, et al. Phytochemical control of poultry coccidiosis: a review. Poult Sci 2022;101:101542. https://doi.org/10.1016/j.psj.2021.101542
  16. Noack S, Chapman HD, Selzer PM. Anticoccidial drugs of the livestock industry. Parasitol Res 2019;118:2009-26. https://doi.org/10.1007/s00436-019-06343-5 
  17. Rybicki MJ. Coccidiostats in treating coccidiosis. Zywnosc Nauka Technologia Jakosc 2020;27:125-37. https://doi.org/10.15193/zntj/2020/125/364
  18. Del Cacho E, Gallego M, Lillehoj HS, et al. IL-17A regulates Eimeria tenella schizont maturation and migration in avian coccidiosis. Vet Res 2014;45:25. https://doi.org/10.1186/1297-9716-45-25
  19. Pastor-Fernandez I, Collantes-Fernandez E, Jimenez-Pelayo L, Ortega-Mora LM, Horcajo P. Modeling the ruminant placenta-pathogen interactions in Apicomplexan parasites: current and future perspectives. Front Vet Sci 2021;7:634458. https://doi.org/10.3389/fvets.2020.634458
  20. Gururajan A, Rajkumari N, Devi U, Borah P. Cryptosporidium and waterborne outbreaks - A mini review. Trop Parasitol 2021;11:11-5. https://doi.org/10.4103/tp.TP_68_20
  21. Nesse LL, Bakke AM, Eggen T, et al. The risk of development of antimicrobial resistance with the use of coccidiostats in poultry diets. Eur J Nutr Food Saf 2019;11:40-3. ID: sea189696. https://doi.org/10.9734/EJNFS/2019/v11i130127
  22. Mnisi CM, Mlambo V, Gila A, et al. Antioxidant and antimicrobial properties of selected phytogenics for sustainable poultry production. Appl Sci 2023;13:99. https://doi.org/10.3390/app13010099
  23. Broom LJ. Evidence-based consideration of dietary 'alternatives' to anticoccidial drugs to help control poultry coccidial infections. World's Poult Sci J 2021;77:43-54. https://doi.org/10.1080/00439339.2021.1873713
  24. Dhaka P, Chantziaras I, Vijay D, et al. Can improved farm biosecurity reduce the need for antimicrobials in food animals? A scoping review. Antibiotics 2023;12:893. https://doi.org/10.3390/antibiotics12050893
  25. Alagawany M, Elnesr SS, Farag MR, et al. Nutritional significance of amino acids, vitamins and minerals as nutraceuticals in poultry production and health - a comprehensive review. Vet Q 2021;41:1-29. https://doi.org/10.1080/01652176.2020.1857887
  26. Tilli G, Laconi A, Galuppo F, Mughini-Gras L, Piccirillo A. Assessing biosecurity compliance in poultry farms: a survey in a densely populated poultry area in north east Italy. Animals 2022;12:1409. https://doi.org/10.3390/ani12111409
  27. Abebe E, Gugsa G. A review on poultry coccidiosis. Abyssinia J Sci Technol 2018;3:1-12.
  28. Chapman HD. A landmark contribution to poultry science-Prophylactic control of coccidiosis in poultry. Poult Sci 2009;88:813-5. https://doi.org/10.3382/ps.2008-00316
  29. Dembitsky VM. Natural polyether ionophores and their pharmacological profile. Mar Drugs 2022;20:292. https://doi.org/10.3390/md20050292
  30. Clarke L, Fodey TL, Crooks SRH, et al. A review of coccidiostats and the analysis of their residues in meat and other food. Meat Sci 2014;97:358-74. https://doi.org/10.1016/j.meatsci.2014.01.004
  31. Muthamilselvan T, Kuo TF, Wu YC, Yang WC. Herbal remedies for coccidiosis control: A review of plants, compounds, and anticoccidial actions. Evid Based Complement Alternat Med 2016;2016:2657981. https://doi.org/10.1155/2016/2657981
  32. Anthony EJ, Bolitho EM, Bridgewater HE, et al. Metallodrugs are unique: Opportunities and challenges of discovery and development. Chem Sci 2020;11:12888-917. https://doi.org/10.1039/D0SC04082G
  33. Miller MA, Zachary JF. Mechanisms and morphology of cellular injury, adaptation, and death. Pathologic Basis of Veterinary Disease. Sixth Ed. St. Louis, MO, USA: Elsevier; 2017. https://doi.org/10.1016/B978-0-323-35775-3.00001-1
  34. Felici M, Tugnoli B, Piva A, Grilli E. In vitro assessment of anticoccidials: methods and molecules. Animals 2021;11:1962. https://doi.org/10.3390/ani11071962
  35. Acharya KP, Acharya N. Alternatives to fight against coccidiosis: A review. Nepalese Vet J 2017;34:152-67. https://doi.org/10.3126/nvj.v34i0.22918
  36. Roila R, Branciari R, Pecorelli I, et al. Occurrence and residue concentration of coccidiostats in feed and food of animal origin; human exposure assessment. Foods 2019;8:477. https://doi.org/10.3390/foods8100477
  37. Abdelhady AY, El-Safty SA, Hashim M, et al. Comparative evaluation of single or combined anticoccidials on performance, antioxidant status, immune response, and intestinal architecture of broiler chickens challenged with mixed Eimeria species. Poult Sci 2021;100:101162. https://doi.org/10.1016/j.psj.2021.101162
  38. Kadykalo S, Roberts T, Thompson M, Wilson J, Lang M, Espeisse O. The value of anticoccidials for sustainable global poultry production. Int J Antimicrob Agents 2018;51:304-10. https://doi.org/10.1016/j.ijantimicag.2017.09.004
  39. Shivaramaiah C, Barta JR, Hernandez VX, Tellez G, Hargis BM. Coccidiosis: recent advancements in the immunobiology of Eimeria species, preventive measures, and the importance of vaccination as a control tool against these Apicomplexan parasites. Vet Med 2014;5:23-34. https://doi.org//10.2147/VMRR.S57839
  40. Lee Y, Lu M, Lillehoj HS. Coccidiosis: Recent progress in host immunity and alternatives to antibiotic strategies. Vaccines 2022;10:215. https://doi.org/10.3390/vaccines10020215
  41. Attree E, Sanchez AG, Jones M, et al. Controlling the causative agents of coccidiosis in domestic chickens; an eye on the past and considerations for the future. CABI Agric Biosci 2021;2:37. https://doi.org/10.1186/s43170-021-00056-5
  42. Williams RB. Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity. Avian Pathol 2005;34:159-80. https://doi.org/10.1080/03079450500112195
  43. Arain MA, Nabi F, Marghazani IB, et al. In ovo delivery of nutraceuticals improves health status and production performance of poultry birds: a review. World's Poult Sci J 2022;78:765-88. https://doi.org/10.1080/00439339.2022.2091501
  44. Lee SH, Lillehoj HS, Jang SI, et al. Effects of in ovo injection with selenium on immune and antioxidant responses during experimental necrotic enteritis in broiler chickens. Poult Sci 2014;93:1113-21. https://doi.org/10.3382/ps.2013-03770
  45. Stadnicka K, Bogucka J, Stanek M, et al. Injection of raffinose family oligosaccharides at 12 days of egg incubation modulates the gut development and resistance to opportunistic pathogens in broiler chickens. Animals 2020;10:592. https://doi.org/10.3390/ani10040592
  46. Pender CM, Kim S, Potter TD, Ritzi MM, Young M, Dalloul RA. Effects of in ovo supplementation of probiotics on performance and immunocompetence of broiler chicks to an Eimeria challenge. Benef Microbes 2016;7:699-705. https://doi.org/10.3920/BM2016.0080
  47. Sokale AO, Zhai W, Pote LM, Williams CJ, Peebles ED. Effects of coccidiosis vaccination administered by in ovo injection on Ross 708 broiler performance through 14 days of posthatch age. Poult Sci 2017;96:2546-51. https://doi.org/10.3382/ps/pex041
  48. Zaheer T, Abbas RZ, Imran M, et al. Vaccines against chicken coccidiosis with particular reference to previous decade: progress, challenges, and opportunities. Parasitol Res 2022;121:2749-63. https://doi.org/10.1007/s00436-022-07612-6
  49. Huang H, Jiang Y, Zhou F, et al. A potential vaccine candidate towards chicken coccidiosis mediated by recombinant Lactobacillus plantarum with surface displayed EtMIC2 protein. Exp Parasitol 2020;215:107901. https://doi.org/10.1016/j.exppara.2020.107901
  50. Yuan B, Sun Z, Lu M, et al. Immunization with pooled antigens for Clostridium perfringens conferred partial protection against experimental necrotic enteritis in broiler chickens. Vaccines 2022;10:979. https://doi.org/10.3390/vaccines10060979
  51. Blake DP, Marugan-Hernandez V, Tomley FM. Spotlight on avian pathology: Eimeria and the disease coccidiosis. Avian Pathol 2021;50:209-13. https://doi.org/10.1080/03079457.2021.1912288
  52. Arczewska-Wlosek A, Swiatkiewicz S, Ognik K, Jozefiak D. Effects of a dietary multi-strain probiotic and vaccination with a live anticoccidial vaccine on growth performance and haematological, biochemical and redox status indicators of broiler chickens. Animals 2022;12:3489. https://doi.org/10.3390/ani12243489
  53. Soutter F, Werling D, Tomley FM, Blake DP. Poultry coccidiosis: design and interpretation of vaccine studies. Front Vet Sci 2020;7:101. https://doi.org/10.3389/fvets.2020.00101
  54. Venkatas J, Adeleke MA. A review of Eimeria antigen identification for the development of novel anticoccidial vaccines. Parasitol Res 2019;118:1701-10. https://doi.org/10.1007/s00436-019-06338-2
  55. Barbour E, Ayyash D, Iyer A, Harakeh S, Kumosani T. A review of approaches targeting the replacement of coccidiostat application in poultry production. Braz J Poult Sci 2015;17:405-18. https://doi.org/10.1590/1516-635x1704405-418
  56. Chapman HD, Rathinam T. Focused review: the role of drug combinations for the control of coccidiosis in commercially reared chickens. Int J Parasitol Drugs Drug Resist 2022;18:32-42. https://doi.org/10.1016/j.ijpddr.2022.01.001
  57. Ahmad R, Yu YH, Hsiao FSH, et al. Probiotics as a friendly antibiotic alternative: assessment of their effects on the health and productive performance of poultry. Fermentation 2022;8:672. https://doi.org/10.3390/fermentation8120672
  58. Abd El-Hack ME, El-Saadony MT, Salem HM, et al. Alternatives to antibiotics for organic poultry production: types, modes of action and impacts on bird's health and production. Poult Sci 2022;101:101696. https://doi.org/10.1016/j.psj.2022.101696
  59. Kovarovic J, Bystricka J, Vollmannova A, Toth T, Brindza J. Biologically valuable substances in garlic (Allium sativum L.) A review. J Cent Eur Agric 2019;20:292-304. https://doi.org/10.5513/JCEA01/20.1.2304
  60. Elmahallawy EK, Fehaid A, El-Shewehy DM, et al. S-methylcysteine ameliorates the intestinal damage induced by Eimeria tenella infection via targeting oxidative stress and inflammatory modulators. Front Vet Sci 2022;8:754991. https://doi.org/10.3389/fvets.2021.754991
  61. Kim DK, Lillehoj HS, Lee SH, Lillehoj EP, Bravo D. Improved resistance to Eimeria acervulina infection in chickens due to dietary supplementation with garlic metabolites. Br J Nutr 2013;109:76-88. https://doi.org/10.1017/S0007114512000530
  62. Jang HJ, Lee HJ, Yoon DK, Ji DS, Kim JH, Lee CH. Antioxidant and antimicrobial activities of fresh garlic and aged garlic by-products extracted with different solvents. Food Sci Biotechnol 2018;27:219-25. https://doi.org/10.1007/s10068-017-0246-4
  63. Bhavaniramya S, Vishnupriya S, Al AMS, Vijayakumar R, Baskaran D. Role of essential oils in food safety: Antimicrobial and antioxidant applications. Grain Oil Sci Technol 2019;2:49-55. https://doi.org/10.1016/j.gaost.2019.03.001
  64. Habibi H, Firouzi S, Nili H, Razavi M, Asadi SL, Daneshi S. Anticoccidial effects of herbal extracts on Eimeria tenella infection in broiler chickens: in vitro and in vivo study. J Parasit Dis 2016;40:401-7. https://doi.org/10.1007/s12639-014-0517-4
  65. Christaki E, Florou PP, Giannenas I, Papazahariadou M, Botsoglou NA, Spais AB. Effect of a mixture of herbal extracts on broiler chickens infected with Eimeria tenella. Anim Res 2004;53:137-44. https://doi.org/10.1051/animres:2004006
  66. Ali M, Chand N, Khan RU, Naz S, Gul S. Anticoccidial effect of garlic (Allium sativum) and ginger (Zingiber officinale) against experimentally induced coccidiosis in broiler chickens. J Appl Anim Res 2019;47:79-84. https://doi.org/10.1080/09712119.2019.1573731
  67. Alnassan AA, Thabet A, Daugschies A, Bangoura B. In vitro efficacy of allicin on chicken Eimeria tenella sporozoites. Parasitol Res 2015;114:3913-5. https://doi.org/10.1007/s00436-015-4637-2
  68. Ezeorba TPC, Chukwudozie KI, Ezema CA, Anaduaka EG, Nweze EJ, Okeke ES. Potentials for health and therapeutic benefits of garlic essential oils: Recent findings and future prospects. Pharmacol Res 2022;3:100075. https://doi.org/10.1016/j.prmcm.2022.100075
  69. Gadelhaq SM, Arafa WM, Abolhadid SM. In vitro activity of natural and chemical products on sporulation of Eimeria species oocysts of chickens. Vet Parasitol 2018;251:12-6. https://doi.org/10.1016/j.vetpar.2017.12.020
  70. Coroian M, Pop LM, Popa V, et al. Efficacy of Artemisia annua against coccidiosis in broiler chickens: a field trial. Microorganisms 2022;10:2277. https://doi.org/10.3390/microorganisms10112277
  71. Hong SC. Artemisia Annua, Artemisinin, ACTs, and malaria control in Africa: tradition, science, and public policy. By Dana G. Dalrymple. Washington DC, USA: Politics and Prose; 2012. J Econ Hist 2014;74:304-6. https://doi.org/10.1017/S0022050714000242
  72. Cai TY, Zhang YR, Ji JB, Xing J. Investigation of the component in Artemisia annua L. leading to enhanced antiplasmodial potency of artemisinin via regulation of its metabolism. J Ethnopharmacol 2017;207:86-91. https://doi.org/10.1016/j.jep.2017.06.025
  73. Li J, Zhang C, Gong M, Wang M. Combination of artemisinin-based natural compounds from Artemisia annua L. for the treatment of malaria: Pharmacodynamic and pharmacokinetic studies. Phytother Res 2018;32:1415-20. https://doi.org/10.1002/ptr.6077
  74. Lang SJ, Schmiech M, Hafner S, et al. Antitumor activity of an Artemisia annua herbal preparation and identification of active ingredients. Phytomedicine 2019;62:152962. https://doi.org/10.1016/j.phymed.2019.152962
  75. De AGF, Horsted K, Thamsborg SM, Kyvsgaard NC, Ferreira JF, Hermansen JE. Use of Artemisia annua as a natural coccidiostat in free-range broilers and its effects on infection dynamics and performance. Vet Parasitol 2012;186:178-87. https://doi.org/10.1016/j.vetpar.2011.11.058
  76. Fatemi A, Asasi K, Razavi SM. Anticoccidial effects of Artemisia annua ethanolic extract: prevention, simultaneous challenge-medication, and treatment. Parasitol Res 2017;116:2581-9. https://doi.org/10.1007/s00436-017-5567-y
  77. Fatemi A, Razavi SM, Asasi K, Goudarzi MT. Effects of Artemisia annua extracts on sporulation of Eimeria oocysts. Parasitol Res 2015;114:1207-11. https://doi.org/10.1007/s00436-014-4304-z
  78. Del Cacho E, Gallego M, Francesch M, Quilez J, SanchezAcedo C. Effect of artemisinin on oocyst wall formation and sporulation during Eimeria tenella infection. Parasitol Int 2010;59:506-11. https://doi.org/10.1016/j.parint.2010.04.001
  79. Jiao J, Yang Y, Liu M, et al. Artemisinin and Artemisia annua leaves alleviate Eimeria tenella infection by facilitating apoptosis of host cells and suppressing inflammatory response. Vet Parasitol 2018;254:172-7. https://doi.org/10.1016/j.vetpar.2018.03.017
  80. Mtenga DV, Ripanda AS. A review on the potential of underutilized Blackjack (Biden pilosa) naturally occurring in subSaharan Africa. Heliyon 2022;8:e09586. https://doi.org/10.1016/j.heliyon.2022.e09586
  81. Uysal S, Ugurlu A, Zengin G, et al. Novel in vitro and in silico insights of the multi-biological activities and chemical composition of Bidens tripartita L.. Food Chem Toxicol 2018;111:525-36. https://doi.org/10.1016/j.fct.2017.11.058
  82. Chang CLT, Yang CY, Muthamilselvan T, Yang WC. Field trial of medicinal plant, Bidens pilosa, against eimeriosis in broilers. Sci Rep 2016;6:24692. https://doi.org/10.1038/srep24692
  83. Yang MT, Lin YX, Yang G, et al. Functional and mechanistic studies of two anti-coccidial herbs, Bidens pilosa and Artemisia indica. Planta Med 2022;88:282-91. https://doi.org/10.1055/a-1527-9715
  84. Khater HF, Ziam H, Abbas A, et al. Avian coccidiosis: Recent advances in alternative control strategies and vaccine development. Agrobiol Rec 2020;1:11-25. https://doi.org/10.47278/journal.abr/2020.003
  85. Memon FU, Yang Y, Lv F, et al. Effects of probiotic and Bidens pilosa on the performance and gut health of chicken during induced Eimeria tenella infection. J Appl Microbiol 2021; 131:425-34. https://doi.org/10.1111/jam.14928
  86. Bozkurt M, Ege G, Aysul N, et al. Effect of anticoccidial monensin with oregano essential oil on broilers experimentally challenged with mixed Eimeria spp. Poult Sci 2016;95:1858-68. https://doi.org/10.3382/ps/pew077
  87. Abdelli N, Sola-Oriol D, Perez JF. Phytogenic feed additives in poultry: Achievements, prospective and challenges. Animals 2021;11:3471. https://doi.org/10.3390/ani11123471
  88. Tsinas A, Giannenas I, Voidarou C, Tzora A, Skoufos J. Effects of an oregano based dietary supplement on performance of broiler chickens experimentally infected with Eimeria acervulina and Eimeria maxima. J Poult Sci 2011;48:194-200. https://doi.org/10.2141/jpsa.010123
  89. Mohiti-Asli M, Ghanaatparast-Rashti M. Dietary oregano essential oil alleviates experimentally induced coccidiosis in broilers. Prev Vet Med 2015;120:195-202. https://doi.org/10.1016/j.prevetmed.2015.03.014
  90. Murakami AE, Eyng C, Torrent J. Effects of functional oils on coccidiosis and apparent metabolizable energy in broiler chickens. Asian-Australas J Anim Sci 2014;27:981-9. https://doi.org/10.5713/ajas.2013.13449
  91. Jeldi L, Taarabt KO, Mazri MA, Ouahmane L, Alfeddy MN. Chemical composition, antifungal and antioxidant activities of wild and cultivated Origanum compactum essential oils from the municipality of Chaoun, Morocco. S Afr J Bot 2022;147:852-8. https://doi.org/10.1016/j.sajb.2022.03.034
  92. Gadde U, Kim WH, Oh ST, Lillehoj HS. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review. Anim Health Res Rev 2017;18:26-45. https://doi.org/10.1017/S1466252316000207
  93. Assis RCL, Luns FD, Beletti ME, et al. Histomorphometry and macroscopic intestinal lesions in broilers infected with Eimeria acervulina. Vet Parasitol 2010;168:185-9. https://doi.org/10.1016/j.vetpar.2009.11.017
  94. Santos RR, Velkers FC, Vernooij JCM, et al. Nutritional interventions to support broiler chickens during Eimeria infection. Poult Sci 2022;101:101853. https://doi.org/10.1016/j.psj.2022.101853
  95. Lan Y, Xun S, Tamminga S, Williams B, Verstegen M, Erdi G. Real-time PCR detection of lactic acid bacteria in cecal contents of Eimeria tenella-lnfected broilers fed soybean oligosaccharides and soluble soybean polysaccharides. Poult Sci 2004;83:1696-702. https://doi.org/10.1093/ps/83.10.1696
  96. Adhikari P, Kiess A, Adhikari R, Jha R. An approach to alternative strategies to control avian coccidiosis and necrotic enteritis. J Appl Poult Res 2020;29:515-34. https://doi.org/10.1016/j.japr.2019.11.005
  97. Chand N, Faheem H, Khan RU, Qureshi MS, Alhidary IA, Abudabos AM. Anticoccidial effect of mananoligosacharide against experimentally induced coccidiosis in broiler. Environ Sci Pollut Res 2016;23:14414-21. https://doi.org/10.1007/s11356-016-6600-x
  98. McCann M, Newell E, Preston C, Forbes K. The use of mannanoligosaccharides and/or tannin in broiler diets. Int J Poult Sci 2006;5:873-9. https://doi.org/10.3923/ijps.2006.873.879
  99. Ritzi MM, Abdelrahman W, Mohnl M, Dalloul RA. Effects of probiotics and application methods on performance and response of broiler chickens to an Eimeria challenge. Poult Sci 2014;93:2772-8. https://doi.org/10.3382/ps.2014-04207 
  100. Yin G, Lin Q, Wei W, et al. Protective immunity against Eimeria tenella infection in chickens induced by immunization with a recombinant C-terminal derivative of EtIMP1. Vet Immunol Immunopathol 2014;162:117-21. https://doi.org/10.1016/j.vetimm.2014.10.009 
  101. Wang X, Farnell YZ, Kiess AS, Peebles ED, Wamsley KG, Zhai W. Effects of Bacillus subtilis and coccidial vaccination on cecal microbial diversity and composition of Eimeriachallenged male broilers. Poult Sci 2019;98:3839-49. https://doi.org/10.3382/ps/pez096 
  102. Lee SH, Lillehoj HS, Dalloul RA, Park DW, Hong YH, Lin JJ. Influence of Pediococcus-based probiotic on coccidiosis in broiler chickens. Poult Sci 2007;86:63-6. https://doi.org/10.1093/ps/86.1.63 
  103. Castro FLS, Tompkins YH, Pazdro R, Kim WK. The effects of total sulfur amino acids on the intestinal health status of broilers challenged with Eimeria spp. Poult Sci 2020;99:5027-36. https://doi.org/10.1016/j.psj.2020.06.055 
  104. Teng PY, Choi J, Tompkins Y, Lillehoj H, Kim W. Impacts of increasing challenge with Eimeria maxima on the growth performance and gene expression of biomarkers associated with intestinal integrity and nutrient transporters. Vet Res 2021;52:81. https://doi.org/10.1186/s13567-021-00949-3 
  105. Jankowski J, Kubinska M, Juskiewicz J, Czech A, Ognik K, Zdunczyk Z. Effect of different dietary methionine levels on the growth performance and tissue redox parameters of turkeys. Poult Sci 2017;96:1235-43. https://doi.org/10.3382/ps/pew383 
  106. Duangnumsawang Y, Zentek J, Boroojeni FG. Development and functional properties of intestinal mucus layer in poultry. Front Immunol 2021;12:745849. https://doi.org/10.3389/fimmu.2021.745849 
  107. Zhang Q, Chen X, Eicher SD, Ajuwon KM, Applegate TJ. Effect of threonine deficiency on intestinal integrity and immune response to feed withdrawal combined with coccidial vaccine challenge in broiler chicks. Br J Nutr 2016;116:2030-43. https://doi.org/10.1017/S0007114516003238 
  108. Chen YP, Cheng YF, Li XH, et al. Effects of threonine supplementation on the growth performance, immunity, oxidative status, intestinal integrity, and barrier function of broilers at the early age. Poult Sci 2017;96:405-13. https://doi.org/10.3382/ps/pew240 
  109. Sarwar MS, Zhang HJ, Tsang SW. Perspectives of plant natural products in inhibition of cancer invasion and metastasis by regulating multiple signaling pathways. Curr Med Chem 2018;25:5057-87. https://doi.org/10.2174/0929867324666170918123413
  110. Quinteros JA, Scott PC, Wilson TB, et al. Isoquinoline alkaloids induce partial protection of laying hens from the impact of Campylobacter hepaticus (spotty liver disease) challenge. Poult Sci 2021;100:101423. https://doi.org/10.1016/j.psj.2021.101423 
  111. Li JY, Huang HB, Pan TX, et al. Sanguinarine induces apoptosis in Eimeria tenella sporozoites via the generation of reactive oxygen species. Poult Sci 2022;101:101771. https://doi.org/10.1016/j.psj.2022.101771 
  112. Xu X, Yi H, Wu J, et al. Therapeutic effect of berberine on metabolic diseases: Both pharmacological data and clinical evidence. Biomed Pharmacother 2021;133:110984. https://doi.org/10.1016/j.biopha.2020.110984 
  113. Zhu C, Huang K, Bai Y, et al. Dietary supplementation with berberine improves growth performance and modulates the composition and function of cecal microbiota in yellow-feathered broilers. Poult Sci 2021;100:1034-48. https://doi.org/10.1016/j.psj.2020.10.071 
  114. Yuan L, Li M, Qiao Y, Wang H, Cui L, Wang M. The impact of berberine on intestinal morphology, microbes, and immune function of broilers in response to necrotic enteritis challenge. BioMed Res Int 2021;2021:1877075. https://doi.org/10.1155/2021/1877075 
  115. Nguyen BT, Flores RA, Cammayo PLT, Kim S, Kim WH, Min W. Anticoccidial activity of berberine against Eimeria-infected chickens. Korean J Parasitol 2021;59:403-8. https://doi.org/10.3347/kjp.2021.59.4.403 
  116. Huang Q, Liu X, Zhao G, Hu T, Wang Y. Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Anim Nutr 2018;4:137-50. https://doi.org/10.1016/j.aninu.2017.09.004 
  117. Mahlake SK, Mnisi CM, Kumanda C, Mthiyane DMN, Montso PK. Green tea (Camellia sinensis) products as alternatives to antibiotics in poultry nutrition: A Review. Antibiotics 2022;11:565. https://doi.org/10.3390/antibiotics11050565 
  118. Tonda RM, Rubach JK, Lumpkins BS, Mathis GF, Poss MJ. Effects of tannic acid extract on performance and intestinal health of broiler chickens following coccidiosis vaccination and/or a mixed-species Eimeria challenge. Poult Sci 2018;97: 3031-42. https://doi.org/10.3382/ps/pey158 
  119. Wang M, Suo X, Gu J, Zhang W, Fang Q, Wang X. Influence of grape seed proanthocyanidin extract in broiler chickens: effect on chicken coccidiosis and antioxidant status. Poult Sci 2008;87:2273-80. https://doi.org/10.3382/ps.2008-00077 
  120. Choi J, Tompkins YH, Teng PY, Gogal Jr RM, Kim WK. Effects of tannic acid supplementation on growth performance, oocyst shedding, and gut health of in broilers infected with Eimeria maxima. Animals 2022;12:1378. https://doi.org/10.3390/ani12111378 
  121. Lako JDW, Sube KLL, Lumori CSG, et al. Diversity and distribution of medicinal plants in the republic of South Sudan. World J Adv Res Rev 2020;7:18-31. https://doi.org/10.30574/wjarr.2020.7.1.0165 
  122. Batiha GES, Akhtar N, Alsayegh AA, et al. Bioactive compounds, pharmacological actions, and pharmacokinetics of genus Acacia. Molecules 2022;27:7340. https://doi.org/10.3390/molecules27217340 
  123. Ahmed E, Galal M, Abdelmageed N, et al. An in vitro evaluation of the inhibitory effects of an aqueous extract of Acacia nilotica on Eimeria tenella. SVU-Int J Vet Sci 2022;5:33-40. 
  124. Cheng YH, Horng YB, Dybus A, Yu YH. Bacillus licheniformis-Fermented Products improve growth performance and intestinal gut morphology in broilers under Clostridium perfringens challenge. J Poult Sci 2021;58:30-9. https://doi.org/10.2141/jpsa.0200010 
  125. Lee TY, Lee YS, Yeh RH, Chen KH, Chen KL. Bacillus amyloliquefaciens CU33 fermented feather meal-soybean meal product improves the intestinal morphology to promote the growth performance of broilers. Poult Sci 2022;101:102027. https://doi.org/10.1016/j.psj.2022.102027 
  126. Cheng YH, Horng YB, Chen WJ, et al. Development and validation the efficacy of Bacillus-based fermented products as an antibiotics alternative in domestic animals. Acta Sci Pol Zootech 2021;20:23-34. https://doi.org/10.21005/asp.2021.20.3.03 
  127. Cheng YH, Horng YB, Chen WJ, Hua KF, Dybus A, Yu YH. Effect of fermented products produced by Bacillus licheniformis on the growth performance and cecal microbial community of broilers under coccidial challenge. Animals 2021;11:1245. https://doi.org/10.3390/ani11051245 
  128. Yu YH, Wu CM, Chen WJ, Hua KF, Liu JR, Cheng YH. Effectiveness of Bacillus licheniformis-fermented products and their derived antimicrobial lipopeptides in controlling coccidiosis in broilers. Animals 2021;11:3576. https://doi.org/10.3390/ani11123576 
  129. Cheng YH, Zhang N, Han JC, Chang CW, Hsiao FSH, Yu YH. Optimization of surfactin production from Bacillus subtilis in fermentation and its effects on Clostridium perfringens-induced necrotic enteritis and growth performance in broilers. J Anim Physiol Anim Nutr 2018;102:1232-44. https://doi.org/10.1111/jpn.12937