Abstract
The purpose of the present experiment was to explore the therapeutic effect of the crude fruit juice of Citrus aurantifolia (CAJ) on Eimeria tenella disorder in chickens. One hundred twenty 3-week-old Ross 308 broilers of equal sexes were assigned to six experimental groups of 20 birds each. Groups A, B, C, D, and E were experimentally infected with 20,000 sporulated Eimeria tenella oocysts. Broilers in groups A, B, and C were infected and allocated to three treatment-graded doses of C. aurantifolia fruit juice (20, 10, and 5 mL/kg body weight, respectively) which were administered orally for 7 consecutive days of the trial. Group D was infected and treated with a reference drug, Amprolium 1.5 g/L of drinking water (positive control), group E served as infected-untreated control, and group F was uninfected and non-treated (negative control). Oocysts per gram of feces were counted using the McMaster counting device, weight gain was calculated, and blood samples from each experimental group were collected on days 0, 7, 14, 21, and 28 post-infection for hematological evaluation. Results revealed that medication of broilers with C. aurantifolia fruit juice dose-dependently increased body weight, improved cecal lesion, decreased the E. tenella oocyst production rate, and significantly (P<0.05) increased the PCV of the infected broilers. C. aurantifolia provided valuable therapeutic effects against E. tenella–induced coccidiosis in broiler chickens. The plant fruit juice should be further validated to explore the vital compounds responsible for the anticoccidial efficacy.
Similar content being viewed by others
Data availability
The datasets generated and/or analyzed during the current study are not publicly available due to cooperating producer privacy and confidentiality but are available from the corresponding author on reasonable request.
References
Abbas, R.Z., Abbas, A., Iqbal, Z., Raza, M.A., Hussain, K., Ahmed, T. and Shafi, M.U. 2020a. In vitro anticoccidial activity of Vitis vinifera extract on oocysts of different Eimeria species of Broiler Chicken. Journal Hellenic, Veterinary Medical Society, 71(3), 2267-2272.
Abbas, R.Z., Iqbal, Z., Khan, A., Sindhu, Z.U.D., Khan, J.A., Khan, M.N. and Raza, A. 2020b. Options for integrated strategies for the control of avian coccidiosis. International Journal of Agricultural Biology, 14, 1014–1020.
Adem, D.M. and Ame, M.M. 2023. Prevalence of Poultry Coccidiosis and its associated risk factors in and around Haramaya District, Ethiopia. Veterinary Medicine Open Journal, 8 (1), 9 – 17.
Ahad, S., Tanveer, S., Malik, T.A. and Nawchoo, I. A. 2018. Anticoccidial Activity of Fruit Peel of Punica granatum L, Microbial Pathogenesis, 116, 78–83.
Ahmed, A.I., Sulaiman, M.M., Istifanus, W.A., Panda, S.M. and chongmobmi, M. 2019. Anticoccidial Efficacy of Azadirachta Indica Leaf Powder against Eimeria tenella infection in broiler chickens. Journal of Pure and Applied Science, 16, 82–88.
Ali, M., N Chand, N., Khan, R.U., Naz, S. and Gul, S. 2019. Anticoccidial effect of garlic (Allium sativum) and ginger (Zingiber officinale ) aginst experimentally induced coccidiosis in broiler chickens, Journal of Applied Animal Research, 47 (1), 79–84 .
Aljedale, M.M. and Al-Malki, E.S. 2020. Anticoccidial Activities of Salvadora persica (arak) Zin-giber officinale (ginger) and Curcuma longa (turmeric) Extracts on the Control of Chicken Coccidiosis, Journal of King Saud University of Sciences, 32, 2810–2817.
Arya, S.S., Nachiappan, N., Waghmare, R. and Bhat, M.S. 2023. Recent progress and future perspectives on non-thermal apple juice processing techniques, Food Production process and Nutrition, 5, 36. https://doi.org/10.1186/s43014-023-00149-w
Ashraf, S., Bhatti, S.A., Nawaz, H. and Khan, M.S. 2020. Assessment of dietary selenium sources in commercial male broiler breeders: effects on semen quality, antioxidant status and immune responses. Pakistan Veterinary Journal, 40, 13-18.
Asrar, B., Khan, I.U., Homberg, J.R. and Haleem, D.J. 2020. Nigella sativa oil ameliorates chronic ethanol induced anxiety and impaired spatial memory by modulating noradrenaline levels. Pakistan Veterinary Journal, 40, 350-354.
Chaughule, R.S. and Barve, R.S. 2023. Role of herbal medicines in the treatment of infectious diseases. Vegetos, https://doi.org/10.1007/s42535-022-00549-2
Chen, S., Xiaojing, W., Yu C., Hongsheng G. and Xuehao, C. 2023. "A Review of Classification, Biosynthesis, Biological Activities and Potential Applications of Flavonoids" Molecules 28, 13, 4982. https://doi.org/10.3390/molecules28134982
Cheng, P., Wu, Y., Guo, S., Ma, X., Fei, C., Xue, F., Zhu, C., Wang, M., Feng Gu, F. 2022. RPA assay coupled with CRISPR/Cas12a system for the detection of seven Eimeria species in chicken fecal samples. Veterinary Parasitology, 311,109810. https://doi.org/10.1016/j.vetpar.2022.109810.
Cheru, H., Tamrat, H., Hailemelekot, M., Cassini, R. and Belayneh, N. 2023. Epidemiology and identification of Eimeria species affecting poultry in East Gojjam Zone, North West Ethiopia. Journal of Veterinay Medical Science, 9(5), 2160 -2167. https://doi.org/10.1002/vms3.1243.
Coles, G.C. (eds), (1986). Anthelminthic resistance in sheep. In: Gibbs, H.C., Herd, R.P. and Murrell, K.D. (eds), Veterinary Clinics of North America. Food Animal Practice. Philadelphia: Saunders, W.B, 423–432.
Crawley, M. 1993. GLIM for Ecologists. Blackwell Scientific, Oxford.
Dakpogan, H.B., Mensah, S., Attindehou, S., Chysostome, C., Aboh, A., Naciri, M. and Mensah, G.A. 2019. Anticoccidial activity of Carica papaya and Vernonia amygdalina extract. International Journal of Biology and Chemistry Science, 12, 2101.
Desalegn, A.Y. and Ahmed, M.R. 2020. Anticoccidial activity of Aloe debrana and Aloe pulcherrima leaf gel against Eimeria oocysts. Journal of Parasitology Research, 1, 1-10.
Durry, K.A.B. and Wallington, E.A. 1976. Histological technique. Histology, 4, 48–58.
Food and Agriculture Organisation (FAO). The State of Food Security and Nutrition in the World 2020. Available online: https://www.fao.org/publications/sofi/2020. Accessed 12 July 2022.
Freitas, L.F.V.D., Sakomura, N.K., Reis, M.P., Mariani, A.B., Lambert, W., Andretta, I. and Létourneau-Montminy, M.P. 2023. Coccidiosis infection and growth performance of broilers in experimental trials: insights from a meta-analysis including modulating factors. Journal of Poultry Science, 102(11), 103021. https://doi.org/10.1016/j.psj.2023.103021.
Gadelhaq, S.M., Arafa, W.M. and Abolhadid, S.M. 2018. In vitro activity of natural and chemical products on sporulation of Eimeria species oocysts of chickens. Veterinary Parasitology, 251, 12-16.
Galovičová, L., Borotová, P., Vukovic, N.L., Vukic, M., Kunová, S., Hanus, P., Kowalczewski, P.Ł., Bakay, L. and Kačániová, M. 2022. The Potential Use of Citrus aurantifolia L. Essential Oils for Decay Control, Quality Preservation of Agricultural Products, and Anti-Insect Activity. Agronomy, 12, 735. https://doi.org/10.3390/agronomy12030735. [Google Scholar]
Ghafouri, S.A., Ghaniei, A., Tamannaei, A.E.T., Sadr, S., Charbgoo, A., Ghiassi, S. and Abuali, M. 2023. Evaluation of therapeutic effects of an herbal mixture (Echinacea purpurea and Glycyrrhiza glabra) for treatment of clinical coccidiosis in broilers. Journal of Veterinary Medical Science, 9(2), 829-836. https://doi.org/10.1002/vms3.971.
Harbourne, J.B. (1983). Phytochemical Methods: A Guide to Modern Technique of plants Analysis. Chapman and Hall, London.
Haug, A., Williams, R.B. and Larsen, S. 2006. Counting coccidial oocysts in chicken faeces: A comparative study of a standard McMaster technique and a new rapid method. Veterinary Parasitology, 136 (3-4), 233-242.
Hendrix, T. 2022. Sustainable breeding in poultry industry; 6th Edition of Poultry world. Available online: https://www.poultryworld.net/the-industrymarkets/market-trends-analysis-the-industrymarkets-2/poultryworld-edition-6-of-2022. Accessed 19 Sep 2022.
Ibrahim, A., Yahya, M.M. and Usman, B.S. 2018. Effects of Dietary Levels of Doum Palm Pulp Meal (Hyphaene thabaica) Supplementation on the Performance of Broiler Chickens. Asian Journal of Research in Animal and Veterinary Science, 2, 1–8.
Imran, A. and Alsayeqh, A. 2022. Anticoccidial efficacy of Citrus sinensis essential oil in broiler chickens. Pakistan Veterinary Journal, 42, 461 – 466. https://doi.org/10.29261/pakvetj/082.
Indriyani, N.N, Jamaludin, A., Nandang, P., Sarifah, N. and Euis, J. 2023. "Bioactive Components and Their Activities from Different Parts of Citrus aurantifolia (Christm.) Swingle for Food Development" Foods 12(10), 2036. https://doi.org/10.3390/foods12102036
Ishaq, A.N., Sani, D., Abdullahi, S.A. and Jatua, D. 2022. In vitro Anticoccidial activity of ethanolic leaf extract of Citrus aurantium L. against Eimeria tenella oocysts. Sokoto Journal of Veterinary science, 20, 37 – 43.
Jeffrey, J. 2022. Antibacterial Potential of Lime (Citrus aurantifolia) on The Growth of Streptococcus Mutans. Journal. Health and Dental Science,1, 185–194. https://doi.org/10.54052/jhds.sd22.p185-194. [Google Scholar]
Kaingu, F., Liu, D., Wang, L., Tao, J., Waihenya, R. and Kutima, H. 2017. Anticoccidial Effects of Aloe secundiflora Leaf Extract Against Eimeria tenella in Broiler Chicken. Tropical Animal Health Production, 49, 823–828.
Kauffmann, A.C. and Vinicius, S.C. 2023. "Phenolic Compounds in Bacterial Inactivation: A Perspective from Brazil" Antibiotics 12, 4, 645. https://doi.org/10.3390/antibiotics12040645
Kazeem, M.I., Bankole, H.A., Oladokun, T.I., Bello, A.O. and Maliki, M.A. 2020. Citrus aurantifolia (Christm.) Swingle (Lime) Fruit Extract Inhibits the Activities of Polyol Pathway Enzymes. EFood, 1, 310–315. [Google Scholar]
Khaskheli, A.A., Khaskheli, M.I., Khaskheli, A.J. and Khaskheli, A.A. 2020. Dietary influence of Yucca schidigera on broilers and layers: A review. International Journal of Veterinary Science, 9, 458-461.
Khater, H.F., Ziam, H., Abbas, A., Hussain, K., Zahid, R., Raza M.A., Younis, E.Z., Radwan, I.T. and Selim, A. 2020. Avian coccidiosis: Recent advances in alternative control strategies and vaccine development. Agrobiological Records, 1, 11-25.
Lopez-Corona, A.V., Valencia-Espinosa, I., González-Sánchez, F.A., Sánchez-López, A.L., Garcia-Amezquita, L.E. and Garcia-Varela R. 2022. Antioxidant, Anti-Inflammatory and Cytotoxic Activity of Phenolic Compound Family Extracted from Raspberries (Rubus idaeus): A General Review. Antioxidants (Basel). 11(6), 1192. https://doi.org/10.3390/antiox11061192.
Lorke, D. 1983. A new approach to acute toxicity testing. Archives of Toxicology, 53, 275–287.
Mahmoud, K., Morsy, M.A., Abd El-Lateef, H.M., Marzok, M., El-Beltagi, H.S., Al Khodair, K.M., Albokhadaim, I., Venugopala, K.N., Al-Rasheed, M. and Ismail, M.M. 2023. A century of “anticoccidial drugs”: bibliometric analysis. Frontier in Veterinary Science, 10:1157683. https://doi.org/10.3389/fvets.2023.1157683
Mahmoud, R.E., Elshopakey, G.E. and Awadin, W.F. 2020. Effects of feeding diets supplemented with different levels of l-carnitine on growth performance, serum metabolites, histopathological changes in growing Japanese quails. International Journal of Veterinary Science, 9, 16-23.
Mares, M.M., Saleh, A., Rewaida, A., and Mutee, M. 2023. "Morphological and Molecular Characterization of Eimeria spp. Infecting Domestic Poultry Gallus gallus in Riyadh City, Saudi Arabia". Microorganisms 11, 3, 795. https://doi.org/10.3390/microorganisms11030795
Mohamed, E.R.A., Elazab, M.F., El-Habashi, N., Elhawary, N. and Mokhbatly, A.A. 2021. Anticoccidial Effect of Origanum majorana Aqueous Extract on Eimeria tenella -infected Chicken, Tropical Biomedicine, 38, 62–72.
Monjur, A. 2023. Intestinal parasitic Infections in 2023. Gastroenterology Research, 16(3), 127 – 140.
Morehouse, N.F. and Baron, R.R. 1970. Coccidiosis: evaluation of coccidiostats by mortality weight gains and faecal scores. Experimental Parasitology, 28 (1), 25–29.
Moryani, A.A., Rajput, N., Naeem, M., Shah, A.H. and Jahejo, A.R. 2021. Screening of the Herbs and Evaluation of Their Combined Effects on the Health and Immunity of Coccidiosis Challenged Broiler Chickens. Pakistan Veterinary Journal, 41, 228-234.
Murshed, M., Aljawdah, H.M.A., Mares, M. and Al-Quraishy, S. 2023. In Vitro: The Effects of the Anticoccidial Activities of Calotropis procera Leaf Extracts on Eimeria stiedae Oocysts Isolated from Rabbits. Molecules, 10, 28(8), 3352. https://doi.org/10.3390/molecules28083352
Nworah, F.N., Chukwuma, I.F., Nwanelo, V.O., Osuji, D.O., Onyeso, S.S., Iwuji, G.O., Ngwu, L.N., Odo, C.P., Okoroafor, C.C., Nkwocha, A.C., Ezeako, E.C. 2022. Gastroprotective effect of aqueous Achatina achatina L. (snail) slime extract on indomethacin- and acidified ethanol-induced ulceration in wistar albino rats, Pakistan Veterinary Journal, 42(4), 571– 575. https://doi.org/10.29261/pakvetj/2022.071.
Obadoni, B.O. and Ochuko, P.O. 2001. Phytochemical studies and cooperative efficacy of the crude extract of some homeostatic plant in Edo and Delta State of Nigeria. Journal of Pure and Applied Science, 8, 203-208.
Oikeh, E.I., Oriakhi, K. and Omoregie, E.S. 2013. Proximate analysis and phytochemical screening of Citrus Sinensis fruit wastes. University of Benin, 1(2), 164-170.
Pawestri, W., Nuraini, D.M. and Andityas, M. 2020. The estimation of economic losses due to coccidiosis in broiler chickens in Central Java, Indonesia. IOP Conference Service. Earth Environmental Science, 411, 1-5.
Petruzzello, M. 2023. Plant and Environmental science. Encyclopaedia Britannica.
Phucharoenrak, P., Muangnoi, C. and Trachootham, D. 2022. A Green Extraction Method to Achieve the Highest Yield of Limonin and Hesperidin from Lime Peel Powder (Citrus aurantifolia). Molecules, 27, 820. https://doi.org/10.3390/molecules27030820.
Qamar, H., Li, A., Zeng, Z., Wang, Y., Mehmood, K., Waqas M., Iqbal, M., Zhang J., Li, J. and Wang, Z.Z. 2020. Effect of grapeseed extract on tibial dyschondroplasia incidence, liver weight, and tibial angiogenesis in chickens. Pakistan Veterinary Journal, 40, 187 – 194.
Ramadaini, K., Azizah, Z., Zulharmita, Z. and Rivai, H. 2020. Overview of Pharmacology and Product Development of Lime (Citrus aurantifolia) Rind. International Journal of Pharmaceutical Science and Medicine, 5, 35–45. [Google Scholar]
Rani, Z., Abbas, R.Z., Abbas, A., Saeed, Z., Rehman, T., Hussain, K.M., Rehman, A. and Hussain, K. 2021. In vitro and In vivo Anticoccidial Effects of Butyric Acid and its Impact on Blood and Serum Chemistry of Broiler Chickens. Kafkas Univasiti Veterina, FakDergisi, 27, 583–588.
Sebghatollahi, Z., Ghanadian, M., Agarwal, P., Ghaheh, H.S., Mahato, N. and Yogesh, R. 2022. Citrus flavonoids: Biological activities, implementation in skin health, and topical applications: A Review. ACS Food Sciences Technology, 2, 1417–1432. [Google Scholar]
Evans, W.C. and Trease, G.E. 2002. Phytochemicals: In: Pharmacognosy, 15th Edition, Saunders Publishers, London, 42–393.
Ugwuoke, G.M. and Pewan, S. 2020. Effect of Methanol Extract of Parkia biglobosa Root Bark on Organ and Carcass Weight and Histopathological Changes in Eimeria tenella Infected Broiler Chickens, Animal Research International, 17, 3587–3595.
Wajiha, G., Qureshi, N.A. and Afridi, R. 2021. Comparative analysis of egg adapted vaccines and salinomycin against coccidiosis in chicks. Microbiology and Pathology, 123, 454-60.
Wiedosari, E. and Wardhana, A.H. 2017. Anticoccidial Activity of Artemisinin and Extract of Artemisia annua Leaves in Chickens Infected by Eimeria tenella. Indonesian Journal of Animal and Veterinary Science, 22, 196–204.
Yi, Y., Yao, M., Sun, P., Cheng, J., Khan, A., Guo, J., Li, H. and Sun, N. 2020. Effect of ethanol extract and fractions of physalis calyx seu fructus on inflammation and Mycoplasma Gallisepticum. Pakistan Veterinary Journal, 40, 283-288.
Zhang, K., Li, X., Na, C., Abbas, A., Abbas, R.Z. and Zaman, M. A. 2020. Anticoccidial effects of Camellia sinensis (green tea) extract and its effect on Blood and Serum chemistry of broiler chickens. Pakistan Veterinary Journal, 40, 77-80.
Zhang, L., Zhang, H., Du, S., Song, X. and Hu, D. 2023. In Vitro Transcriptional Response of Eimeria tenella to Toltrazuril Reveals That Oxidative Stress and Autophagy Contribute to Its Anticoccidial Effect. International Journal of Molecular Sciences, 24(9), 8370. https://doi.org/10.3390/ijms24098370
Zohaib, S. and Khalid, A.A. 2023. Botanicals: A promising Approach for controlling caecal coccidiosis in poultry. Frontiers in Veterinary science. https://doi.org/10.3389/fvets.2023.1157833.
Acknowledgements
The authors acknowledge Mr. Ojoko G. A (National Veterinary research institutive, Plateau State, Nigeria) for the supply of Eimeria oocysts used in this research work.
Author information
Authors and Affiliations
Contributions
Conception and design, material preparation, data collection, and analysis were performed by GU, C.F.O, I.J.O, and I.K.I. The first draft of the manuscript was written by GU and I.K.I. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ugwuoke, G.M., Obi, C.F., Onu, I.J. et al. Therapeutic efficacy of Citrus aurantifolia (lime) juice in experimental Eimeria tenella–infected broiler chickens. Trop Anim Health Prod 56, 8 (2024). https://doi.org/10.1007/s11250-023-03840-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-023-03840-9