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Essential oils alleviate coccidiosis impact in broiler chickens: a meta-analysis

  • Ridho Kurniawan Rusli (Department of Nutrition and Feed Technology, Faculty of Animal Science, Universitas Andalas) ;
  • Melia Afnida Santi (Department of Animal Science, Feed Technology Study Program, Polikteknik Negeri Lampung) ;
  • Nuraini (Department of Nutrition and Feed Technology, Faculty of Animal Science, Universitas Andalas) ;
  • Mustofa Hilmi (Study Program of Livestock Product Processing Technology, Politeknik Negeri Banyuwangi) ;
  • Mirzah (Department of Nutrition and Feed Technology, Faculty of Animal Science, Universitas Andalas) ;
  • Cecep Hidayat (Animal Feed and Nutrition Modelling (AFENUE) Research Group, Department of Nutrition and Feed Technology, Faculty of Animal Science, IPB University) ;
  • Arif Darmawan (Animal Feed and Nutrition Modelling (AFENUE) Research Group, Department of Nutrition and Feed Technology, Faculty of Animal Science, IPB University) ;
  • Khairani (Graduate School of Animal Science, Faculty of Animal Science, Universitas Andalas) ;
  • Rita Mutia (Department of Animal Nutrition and Feed Technology, Faculty of Animal Science, IPB University) ;
  • Mirnawati (Department of Nutrition and Feed Technology, Faculty of Animal Science, Universitas Andalas) ;
  • Anuraga Jayanegara (Animal Feed and Nutrition Modelling (AFENUE) Research Group, Department of Nutrition and Feed Technology, Faculty of Animal Science, IPB University) ;
  • Agung Irawan (Animal Feed and Nutrition Modelling (AFENUE) Research Group, Department of Nutrition and Feed Technology, Faculty of Animal Science, IPB University)
  • 투고 : 2025.04.15
  • 심사 : 2025.06.05
  • 발행 : 2025.12.01

초록

Objective: This meta-analysis aims to examine the efficacy of essential oils (EO) as an anticoccidial alternative on broiler chickens under coccidia challenged trials, focusing on performance indicators including average daily gain (ADG), feed intake (FI), feed conversion ratio (FCR), final body weight (BW), mortality, and intestinal lesion. Methods: A random-effects model was performed using the metafor package in R software. In a subgroup meta-analysis, treatment groups including coccidia-infected birds [C+], C+ group treated with EO [C+EO] or antibiotics [C+AB], and a non-infected control group treated with EO or AB, were compared against the control group [CON]. Results: As expected, C+ birds had lower (p<0.001) final BW and ADG as well as higher (p<0.001) FCR. Administration of either EO or AB on birds with coccidiosis infection resulted in similar final BW, ADG, FI, and FCR with CON birds, suggesting the comparable effectiveness of EO and AB to alleviate the adverse effects of coccidiosis. Broilers on the C+ group exhibited increased small intestine damage as shown by the greater (p<0.001) lesion score, but the mortality was not different from CON and other treatment groups. The Eimeria oocyst count was lower on birds treated with EO than on the infected birds, with an average suppression of 42.11%. Meta-regression demonstrated that C+ birds had inferior FI and ADG than CON and C+EO birds. However, high heterogeneity between studies was identified in all measured outcomes as shown by I2>75%, suggesting wide variability among study conditions. Conclusion: EO may serve as an alternative antibiotic to mitigate the negative impacts of coccidiosis infection in broiler chickens.

키워드

참고문헌

  1. 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
  2. Nasri T, Sangmaneedet S, Nam NH, Worawong K, Taweenan W, Sukon P. Protective efficacy of new-generation anticoccidial vaccine candidates against Eimeria infection in chickens: a meta-analysis of challenge trials. Vet Parasitol 2022;306: 109724. https://doi.org/10.1016/j.vetpar.2022.109724
  3. Eckert J, Carrisosa M, Hauck R. Network meta-analysis comparing the effectiveness of anticoccidial drugs and anticoccidial vaccination in broiler chickens. Vet Parasitol 2021; 291:109387. https://doi.org/10.1016/j.vetpar.2021.109387
  4. Gaignon P, Lambert W, Arnalot L, Fontaine S, ChalvonDemersay T. A combination of functional amino acids and polyphenols can restore the performance of chickens challenged with coccidiosis: a meta-analysis. Anim Open Space 2022;1:100016. https://doi.org/10.1016/j.anopes.2022.100016
  5. Taylor J, Walk C, Misiura M, Sorbara JOB, Giannenas I, Kyriazakis I. Quantifying the effect of coccidiosis on broiler performance and infection outcomes in the presence and absence of control methods. Poult Sci 2022;101:101746. https://doi.org/10.1016/j.psj.2022.101746
  6. Chang L, Di K, Xu J, et al. Effect of natural garlic essential oil on chickens with artificially infected Eimeria tenella. Vet Parasitol 2021;300:109614. https://doi.org/10.1016/j.vetpar.2021.109614
  7. Zhang H, Zhang L, Ren G, et al. Forward genetic analysis of monensin and diclazuril resistance in Eimeria tenella. Int J Parasitol Drugs Drug Resist 2023;22:44-51. https://doi.org/10.1016/j.ijpddr.2023.05.002
  8. Flores RA, Nguyen BT, Cammayo PLT, et al. Epidemiological investigation and drug resistance of Eimeria species in Korean chicken farms. BMC Vet Res 2022;18:277. https://doi.org/10.1186/s12917-022-03369-3
  9. 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
  10. Zhai H, Liu H, Wang S, Wu J, Kluenter AM. Potential of essential oils for poultry and pigs. Anim Nutr 2018;4:179-86. https://doi.org/10.1016/j.aninu.2018.01.005
  11. Di Pasqua R, Betts G, Hoskins N, Edwards M, Ercolini D, Mauriello G. Membrane toxicity of antimicrobial compounds from essential oils. J Agric Food Chem 2007;55:4863-70. https://doi.org/10.1021/jf0636465
  12. Chao SC, Young DG, Oberg CJ. Screening for inhibitory activity of essential oils on selected bacteria, fungi and viruses. J Essent Oil Res 2000;12:639-49. https://doi.org/10.1080/10412905.2000.9712177
  13. Sharmeen Jugreet B, Suroowan S, Rengasamy RRK, Fawzi Mahomoodally M. Chemistry, bioactivities, mode of action and industrial applications of essential oils. Trends Food Sci Technol 2020;101:89-105. https://doi.org/10.1016/j.tifs.2020.04.025
  14. Brenes A, Roura E. Essential oils in poultry nutrition: main effects and modes of action. Anim Feed Sci Technol 2010; 158:1-14. https://doi.org/10.1016/j.anifeedsci.2010.03.007
  15. Nandikatti VL, Poorna Nagasree K, Krishna Kumar MM. Pharmacological activities of essential oils from some flowers, plants and aromatic seeds: a review. J Pharm Biol Sci 2023; 11:72-81. https://doi.org/10.18231/j.jpbs.2023.013
  16. Irawan A, Hidayat C, Jayanegara A, Ratriyanto A. Essential oils as growth-promoting additives on performance, nutrient digestibility, cecal microbes, and serum metabolites of broiler chickens: a meta-analysis. Anim Biosci 2021;34:1499-513. https://doi.org/10.5713/ab.20.0668
  17. Gordillo Jaramillo FX, Kim DH, Lee SH, Kwon SK, Jha R, Lee KW. Role of oregano and citrus species-based essential oil preparation for the control of coccidiosis in broiler chickens. J Anim Sci Biotechnol 2021;12:47. https://doi.org/10.1186/s40104-021-00569-z
  18. Bozkurt M, Selek N, Küçükyilmaz K, et al. Effects of dietary supplementation with a herbal extract on the performance of broilers infected with a mixture of Eimeria species. Br Poult Sci 2012;53:325-32. https://doi.org/10.1080/00071668.2012.699673
  19. Küçükyilmaz K, Bozkurt M, Selek N, et al. Effects of vaccination against coccidiosis, with and without a specific herbal essential oil blend, on performance, oocyst excretion and serum IBD titers of broilers reared on litter. Ital J Anim Sci 2012;11:e1. https://doi.org/10.4081/ijas.2012.e41
  20. Kipper M, Andretta I, Lehnen CR, Lovatto PA, Monteiro SG. Meta-analysis of the performance variation in broilers experimentally challenged by Eimeria spp. Vet Parasitol 2013; 196:77-84. https://doi.org/10.1016/j.vetpar.2013.01.013
  21. Kim E, Létourneau-Montminy MP, Lambert W, ChalvonDemersay T, Kiarie EG. Centennial review: a meta-analysis of the significance of Eimeria infection on apparent ileal amino acid digestibility in broiler chickens. Poult Sci 2022; 101:101625. https://doi.org/10.1016/j.psj.2021.101625
  22. Gurevitch J, Koricheva J, Nakagawa S, Stewart G. Metaanalysis and the science of research synthesis. Nature 2018; 555:175-82. https://doi.org/10.1038/nature25753
  23. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Br Med J 2021;372:n71. https://doi.org/10.1136/bmj.n71
  24. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Testing for heterogeneity. Br Med J 2003;327:557. https://doi.org/10.1136/bmj.327.7414.557
  25. Higgins JPT, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. Br Med J 2011;343:1-9. https://doi.org/10.1136/bmj.d5928
  26. Putra RP, Astuti D, Respati AN, et al. Protective effects of feed additives on broiler chickens exposed to aflatoxins-contaminated feed: a systematic review and meta-analysis. Vet Res Commun 2024;48:225-44. https://doi.org/10.1007/s11259-023-10199-7
  27. McGuinness LA, Higgins JPT. Risk-of-bias VISualization (robvis): an R package and Shiny web app for visualizing riskof-bias assessments. Res Synth Methods 2021;12:55-61. https://doi.org/10.1002/jrsm.1411
  28. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw 2010;36:1-48. https://doi.org/10.18637/jss.v036.i03
  29. Ningsih N, Respati AN, Astuti D, et al. Efficacy of Bacillus subtilis to replace in-feed antibiotics of broiler chickens under necrotic enteritis-challenged experiments: a systematic review and meta-analysis. Poult Sci 2023;102:102923. https://doi.org/10.1016/j.psj.2023.102923
  30. Irawan A, Jayanegara A, Niderkorn V. Impacts of red clover and sainfoin silages on the performance, nutrient utilization and milk fatty acids profile of ruminants: a meta-analysis. J Anim Physiol Anim Nutr 2024;108:13-26. https://doi.org/10.1111/jpn.13853
  31. Irawan A, Sofyan A, Wahyono T, et al. Relationships between dietary rumen-protected lysine and methionine with the lactational performance of dairy cows: a meta-analysis. Anim Biosci 2023;36:1666-84. https://doi.org/10.5713/ab.23.0084
  32. Ahmad R, Yu YH, Hua KF, et al. Management and control of coccidiosis in poultry: a review. Anim Biosci 2024;37:1-15. https://doi.org/10.5713/ab.23.0189
  33. Remmal A, Achahbar S, Bouddine L, Chami N, Chami F. In vitro destruction of Eimeria oocysts by essential oils. Vet Parasitol 2011;182:121-6. https://doi.org/10.1016/j.vetpar.2011.06.002
  34. Almahallawi R, Al-Hoshani N, Al-Nabati EA, et al. Exploring the anticoccidial, growth-promoting, hematological and serological potential activities of Linum usitatissimum essential oil in broiler birds. Pak Vet J 2024;44:117-22. https://doi.org/10.29261/pakvetj/2024.137
  35. Geng T, Peng X, Wu L, et al. Anticoccidial activity of essential oils containing eugenol against Eimeria tenella in broiler chickens. Anim Dis 2024;4:12. https://doi.org/10.1186/s44149-024-00116-z
  36. Freitas LFVB, Sakomura NK, Reis MP, et al. Coccidiosis infection and growth performance of broilers in experimental trials: insights from a meta-analysis including modulating factors. Poult Sci 2023;102:103021. https://doi.org/10.1016/j.psj.2023.103021
  37. Barbalho RLC, Castaneda C, Araújo LF, et al. Β-glucans and MOS, essential oil, and probiotics in diets of broilers challenged with Eimeria spp. and Clostridium perfringens. Poult Sci 2023;102:102541. https://doi.org/10.1016/j.psj.2023.102541
  38. 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
  39. Cahyaningsih U, Satyaningtijas AS, Tarigan R, Nugraha AB. Chicken I-FABP as biomarker of chicken intestinal lesion caused by coccidiosis. IOP Conf Ser Earth Environ Sci 2018; 196:012032. https://doi.org/10.1088/1755-1315/196/1/012032
  40. Kogut MH, Klasing K. An immunologist's perspective on nutrition, immunity, and infectious diseases: introduction and overview. J Appl Poult Res 2009;18:103-10. https://doi.org/10.3382/japr.2008-00080
  41. 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
  42. Moraes PO, Andretta I, Cardinal KM, et al. Effect of functional oils on the immune response of broilers challenged with Eimeria spp. Animal 2019;13:2190-8. https://doi.org/10.1017/S1751731119000600
  43. Jitviriyanon S, Phanthong P, Lomarat P, Bunyapraphatsara N, Porntrakulpipat S, Paraksa N. In vitro study of anti-coccidial activity of essential oils from indigenous plants against Eimeria tenella. Vet Parasitol 2016;228:96-102. https://doi.org/10.1016/j.vetpar.2016.08.020
  44. Upadhaya SD, Cho SH, Chung TK, Kim IH. Anti-coccidial effect of essential oil blends and vitamin D on broiler chickens vaccinated with purified mixture of coccidian oocyst from Eimeria tenella and Eimeria maxima. Poult Sci 2019; 98:2919-26. https://doi.org/10.3382/ps/pez040
  45. 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
  46. Williams RB. Fifty years of anticoccidial vaccines for poultry (1952–2002). Avian Dis 2002;46:775-802. https://doi.org/10.1637/0005-2086(2002)046[0775:fyoavf]2.0.co;2
  47. Kettunen H, Tiihonen K, Peuranen S, Saarinen MT, Remus JC. Dietary betaine accumulates in the liver and intestinal tissue and stabilizes the intestinal epithelial structure in healthy and coccidia-infected broiler chicks. Comp Biochem Physiol A Mol Integr Physiol 2001;130:759-69. https://doi.org/10.1016/S1095-6433(01)00410-x
  48. Kaur G, Athar M, Alam MS. Quercus infectoria galls possess antioxidant activity and abrogates oxidative stress-induced functional alterations in murine macrophages. Chem Biol Interact 2008;171:272-82. https://doi.org/10.1016/j.cbi.2007.10.002
  49. Hamiza OO, Rehman MU, Tahir M, et al. Amelioration of 1,2 dimethylhydrazine (DMH) induced colon oxidative stress, inflammation and tumor promotion response by tannic acid in wistar rats. Asian Pac J Cancer Prev 2012;13:4393-402. https://doi.org/10.7314/apjcp.2012.13.9.4393
  50. Geng T, Ruan X, Xie Y, et al. Anticoccidial activity of a botanical natural product based on eucalyptus, apigenin and eugenol against Eimeria tenella in broiler chickens. Parasit Vectors 2024;17:327. https://doi.org/10.1186/s13071-024-06409-z
  51. Mountzouris KC, Paraskevas V, Tsirtsikos P, et al. Assessment of a phytogenic feed additive effect on broiler growth performance, nutrient digestibility and caecal microflora composition. Anim Feed Sci Technol 2011;168:223-31. https://doi.org/10.1016/j.anifeedsci.2011.03.020
  52. Lee KW, Everts H, Beynen AC. Essential oils in broiler nutrition. Int J Poult Sci 2004;3:738-52. https://doi.org/10.3923/ijps.2004.738.752
  53. Felici M, Tugnoli B, De Hoest-Thompson C, Piva A, Grilli E, Marugan-Hernandez V. Thyme, oregano, and garlic essential oils and their main active compounds influence Eimeria tenella intracellular development. Animals 2024;14:77. https://doi.org/10.3390/ani14010077
  54. Felici M, Tugnoli B, Ghiselli F, et al. Investigating the effects of essential oils and pure botanical compounds against Eimeria tenella in vitro. Poult Sci 2023;102:102898. https://doi.org/10.1016/j.psj.2023.102898
  55. Ewais O, Abdel-Tawab H, El-Fayoumi H, et al. Antioxidant properties of D-limonene and its nanoemulsion form enhance its anticoccidial efficiency in experimentally infected broilers with Eimeria tenella: an in vitro and in vivo study. Vet Res Commun 2024;48:3711-25. https://doi.org/10.1007/s11259-024-10512-y
  56. Elbaz AM, Ashmawy ES, Salama AA, et al. Effects of garlic and lemon essential oils on performance, digestibility, plasma metabolite, and intestinal health in broilers under environmental heat stress. BMC Vet Res 2022;18:430. https://doi.org/10.1186/s12917-022-03530-y
  57. Liu H, Chen P, Lv X, et al. Effects of chlorogenic acid on performance, anticoccidial indicators, immunity, antioxidant status, and intestinal barrier function in coccidia-infected broilers. Animals 2022;12:963. https://doi.org/10.3390/ani12080963
  58. Alp M, Midilli M, Kocabaǧlı N, et al. The effects of dietary oregano essential oil on live performance, carcass yield, serum immunoglobulin G level, and oocyst count in broilers. J Appl Poult Res 2012;21:630-6. https://doi.org/10.3382/japr.2012-00551
  59. Saeed Z, Alkheraije KA. Botanicals: a promising approach for controlling cecal coccidiosis in poultry. Front Vet Sci 2023;10: 1157633. https://doi.org/10.3389/fvets.2023.1157633
  60. Fekam Boyom F, Ngouana V, Amvam Zollo PH, et al. Composition and anti-plasmodial activities of essential oils from some Cameroonian medicinal plants. Phytochemistry 2003; 64:1269-75. https://doi.org/10.1016/j.phytochem.2003.08.004