AbstractThis study investigated the effects of substituting inorganic trace minerals (ITM) with advanced chelate technology-based TM (ACTM) in broiler chicken feed on productive performance, metabolic profile, humoral immunity, antioxidant status, and modulation of NF-kB and Nrf2 signaling pathways in mixed Eimeria species exposure.

摘要本研究调查了在肉鸡饲料中用基于先进螯合技术的TM（ACTM）替代无机微量矿物质（ITM）对生产性能，代谢特征，体液免疫，抗氧化状态以及混合艾美耳球虫暴露中NF-kB和Nrf2信号通路的调节的影响。

The study involved 480 newly hatched male broiler chickens, which were divided into 5 treatment groups, each with 6 replicate cages and 16 chickens per replicate. The experimental treatments included an uninfected negative control group fed a basal diet with recommended inorganic TM levels (NC), an infected positive control group fed the same diet (PC), a PC group supplemented with salinomycin (SAL), and two PC groups in which the basal diet was replaced with 50% and 100% ACTM instead of inorganic TM (ACTM50 and ACTM100, respectively).

该研究涉及480只新孵化的雄性肉鸡，分为5个处理组，每个处理组有6个重复笼，每个重复16只鸡。实验治疗包括未感染的阴性对照组饲喂推荐无机TM水平（NC）的基础饮食，感染的阳性对照组饲喂相同的饮食（PC），PC组补充盐霉素（SAL）和两个PC组，其中基础饮食被50%和100%ACTM代替无机TM（分别为ACTM50和ACTM100）。

All groups, except for the NC group, were orally challenged with mixed Eimeria species oocysts on day 14. According to the results, the PC group showed lower feed intake, breast yield, low-density lipoprotein-cholesterol concentration, lactobacillus spp. counts, and serum IgG levels, but higher jejunal TGF-β expression versus the NC group.

除NC组外，所有组均在第14天用混合艾美耳球虫卵囊进行口服攻击。根据结果，与NC组相比，PC组的采食量，产奶量，低密度脂蛋白胆固醇浓度，乳酸杆菌属计数和血清IgG水平较低，但空肠TGF-β表达较高。

The broilers in the NC, SAL, and ACTM100 groups showed higher body weight gain, carcass yield, and TGF-β expression, but lower serum alkaline phosphatase activity, ileal E. coli count, and jejunal expression levels of IL-1β, IL-6, IFN-γ, Nrf2, and SOD1 compared to the PC group, with the NC group having the highest body weight gain and lowest IL-1β and Nrf2 expression levels.

与PC组相比，NC，SAL和ACTM100组的肉鸡体重增加，胴体产量和TGF-β表达较高，但血清碱性磷酸酶活性，回肠大肠杆菌计数和空肠IL-1β，IL-6，IFN-γ，Nrf2和SOD1的表达水平较低，NC组体重增加最高，IL-1β和Nrf2表达水平最低。

Furthermore, the administration of ACTM100 treatment improved feed efficiency, increased serum iron, zinc, manganese, and copper levels, enhanced total antioxidant capacity and different antioxidant enzy.

此外，ACTM100处理的施用提高了饲料效率，增加了血清铁，锌，锰和铜水平，增强了总抗氧化能力和不同的抗氧化酶。

IntroductionThe genus Eimeria is responsible for coccidiosis, a highly contagious and debilitating condition in poultry. Invasion by Eimeria spp. has also been found to induce oxidative stress within the host. Oxidative stress can harm normal cellular functions, ultimately contributing to the infection’s progression1,2.

引言艾美耳球虫属是引起鸡球虫病的原因，球虫病是一种高度传染性和衰弱性疾病。艾美耳球虫的入侵也被发现在宿主内诱导氧化应激。氧化应激会损害正常的细胞功能，最终导致感染的进展1,2。

The intestinal mucosal epithelium has a vital function in inhibiting the uptake of immunogenic substances. Reducing inflammation and increasing intestinal turnover may enhance the growth rate and feed efficiency of broiler chickens3. Cytokines, as one of the types of cell-secreted proteins in the immune system, play a crucial role in modulating and stimulating the activity of other cells and tissues during inflammation and immune responses.

肠粘膜上皮在抑制免疫原性物质的摄取方面具有重要功能。减少炎症和增加肠道周转可以提高肉鸡的生长速度和饲料效率3。细胞因子作为免疫系统中细胞分泌蛋白的一种，在炎症和免疫反应过程中调节和刺激其他细胞和组织的活性起着至关重要的作用。

Recent studies have shown that coccidiosis infection can result in an increase in nuclear factor kappa B (NF-κB) activity, which in turn leads to the production of pro-inflammatory cytokines4,5. Nuclear factor erythroid 2-related factor (Nrf2), a transcription factor that is sensitive to changes in cellular redox state, enhances the transcription of enzymes involved in antioxidant defense, leading to a decrease in levels of reactive oxygen species (ROS) and inflammation6.

最近的研究表明，球虫病感染可导致核因子κB（NF-κB）活性增加，进而导致促炎细胞因子的产生4,5。核因子红细胞2相关因子（Nrf2）是一种对细胞氧化还原状态变化敏感的转录因子，可增强参与抗氧化防御的酶的转录，导致活性氧（ROS）和炎症水平降低6。

Previous studies show an upregulation of Nrf-2 in response to oxidative stress from the Eimeria challenge, with compensatory increases in antioxidant enzyme expression due to disrupted ecological balance and the need to eliminate excess peroxides1,2.There has been a recent surge of interest in developing dietary solutions that can restore Eimeria anticoccidial sensitivity and maintain optimal broiler performance.

先前的研究表明，响应艾美耳球虫攻击的氧化应激，Nrf-2上调，由于生态平衡中断和需要消除过量的过氧化物，抗氧化酶表达补偿性增加1,2。最近人们对开发饮食解决方案的兴趣激增，可以恢复艾美耳球虫的抗球虫敏感性并保持最佳的肉鸡性能。

One approach that has gained considerable attention is the use of antioxidant compounds for counteracting the harmful effects of ROS produc.

一种备受关注的方法是使用抗氧化剂化合物来抵消ROS产生的有害影响。

Eimeria species challengeAll birds, with the exception of NC, were administered sporulated oocysts of Eimeria species through oral gavage. The birds were administered a solution containing different amounts of oocytes of Eimeria acervulina, Eimeria maxima, and Eimeria tenella on day 1436. Each bird received a dosage of 1 mL.

艾美耳球虫物种挑战者所有鸟类，除NC外，通过口服强饲法给予艾美耳球虫物种的孢子化卵囊。。每只鸟接受1毫升的剂量。

The oocysts of the three different species were acquired from the Laboratory of Parasitology, University of Tehran (Tehran, Iran). The oocysts of these field Eimeria species were obtained from samples of droppings, litter, and intestines of broiler chickens sourced from commercial broiler flocks in Iran.

这三种不同物种的卵囊是从德黑兰大学寄生虫学实验室（伊朗德黑兰）获得的。这些田间艾美耳球虫的卵囊是从伊朗商业肉鸡群的肉鸡粪便，垫料和肠道样本中获得的。

In order to enhance the sporulation process, the oocysts were preserved in a solution of potassium dichromate36. The broiler chickens that were not subjected to any challenges (NC group) were given a 1 mL saline solution, resulting in comparable levels of management stress.Productive performance and samplingThroughout the entire experiment, we recorded the quantity of feed consumed and the weight of the chickens and subsequently calculated the feed efficiency by dividing the body weight gain by the feed intake.

为了增强孢子形成过程，将卵囊保存在重铬酸钾溶液中36。没有受到任何挑战的肉鸡（NC组）被给予1毫升盐水溶液，导致相当程度的管理压力。生产性能和取样在整个实验中，我们记录了消耗的饲料量和鸡的体重，随后通过将体重增加除以采食量来计算饲料效率。

The mortality rate of each cage was recorded on a daily basis and used to adjust performance metrics. On day 42, 2 chickens were chosen from each replication cage, killed through cervical dislocation, and carcasses dissected. The carcass, breast, leg, abdominal fat, and liver weights were measured and expressed as a percentage of the live body weight before slaughter.On day 24 of the experiment, 2 chickens were selected for each replication cage based on the mean body weight of the cage.

每天记录每个笼子的死亡率，并用于调整性能指标。在第42天，从每个复制笼中选择2只鸡，通过颈椎脱位杀死，并解剖尸体。屠宰前测量胴体、胸肉、腿、腹部脂肪和肝脏重量，并表示为活体重的百分比。在实验的第24天，根据笼子的平均体重，为每个复制笼选择2只鸡。

For the purpose of analyzing blood biochemistry, antioxidants, and immunoglobulins, serum samples were acquired by extracting blood from the wing veins of ea.

为了分析血液生化，抗氧化剂和免疫球蛋白，通过从ea的翼静脉中提取血液来获取血清样品。

Data availability

数据可用性

The supplemental information files include all data gathered or analyzed throughout the course of this investigation.

补充信息文件包括在整个调查过程中收集或分析的所有数据。

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Download referencesAcknowledgementsWe thank the Department of Research and Development at Sodour Ahrar Shargh Company for kind support in this project.FundingNot applicable.Author informationAuthor notesKamran Taherpour and Hossein Ali Ghasemi contributed equally to this work.Authors and AffiliationsDepartment of Animal Science, Faculty of Agriculture, Ilam University, Ilam, IranNasim Biabani, Kamran Taherpour & Mohammad Akbari GharaeiDepartment of Animal Science, Faculty of Agriculture and Environment, Arak University, Arak, 38156-8-8349, IranHossein Ali GhasemiDepartment of Research and Development, Sodour Ahrar Shargh Company, Tehran, IranMaryam Hafizi & Mohammad Hassan NazaranAuthorsNasim BiabaniView author publicationsYou can also search for this author in.

下载参考文献致谢我们感谢Sodour Ahrar Shargh公司的研究与开发部门在该项目中的友好支持。资金不适用。作者信息作者注Skamran Taherpour和Hossein Ali Ghasemi对这项工作做出了同样的贡献。作者和附属机构Ilam大学农业学院动物科学系，Ilam，IranNasim Biabani，Kamran Taherpour＆Mohammad Akbari GharaeiDepartment of Animal Science，Faculty of Agriculture and Environment，Arak，38156-8-8349，IranHossein Ali Ghasemi研究与发展系，Sodour Ahrar Shargh Company，Tehran，IranMaryam Hafizi＆Mohammad Hassan NazaranAuthorsNasim Biaview作者出版物您也可以搜索这位作者在。

PubMed Google ScholarKamran TaherpourView author publicationsYou can also search for this author in

PubMed Google ScholarKamran TaherpourView作者出版物您也可以在

PubMed Google ScholarHossein Ali GhasemiView author publicationsYou can also search for this author in

PubMed Google ScholarHossein Ali GhasemiView作者出版物您也可以在

PubMed Google ScholarMohammad Akbari GharaeiView author publicationsYou can also search for this author in

PubMed Google Scholarmahammad Akbari GharaeiView作者出版物您也可以在

PubMed Google ScholarMaryam HafiziView author publicationsYou can also search for this author in

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PubMed Google ScholarContributionsK.T, H.A.G, M.H., and M.H.N. conceived the central idea and designed the experiments. N.B., K.T., and M.A.G. performed the experiments. K.T. and H.A.G analyzed data. N.B., K.T., H.A.G., and M.H.N., wrote the main manuscript text and prepared all the figures.

PubMed谷歌学术贡献SK。T、 H.A.G、M.H.和M.H.N.构思了中心思想并设计了实验。N、 B.，K.T。和M.A.G.进行了实验。K、 T.和H.A.G分析了数据。N、 B.，K.T.，H.A.G.和M.H.N.撰写了主要手稿文本并准备了所有数字。

K.T., H.A.G., and M.H.N. supervised the project. All authors reviewed the manuscript.Corresponding authorsCorrespondence to.

K、 T.，H.A.G.和M.H.N.监督了该项目。所有作者都审阅了手稿。通讯作者通讯。

Kamran Taherpour or Hossein Ali Ghasemi.Ethics declarations

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Competing interests

相互竞争的利益

The authors declare no competing interests.

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Ethics approval

All animal handling techniques were in accordance with Ilam University’s Animal Ethics Committee (approval number: 80/4190).

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Reprints and permissionsAbout this articleCite this articleBiabani, N., Taherpour, K., Ghasemi, H.A. et al. Advanced chelate technology-based trace minerals reduce inflammation and oxidative stress in Eimeria-infected broilers by modulating NF-kB and Nrf2 pathways.

转载和许可本文引用本文Biabani，N.，Taherpour，K.，Ghasemi，H.A。等人。基于先进螯合技术的微量矿物质通过调节NF-kB和Nrf2途径减少艾美耳球虫感染肉鸡的炎症和氧化应激。

Sci Rep 14, 24227 (2024). https://doi.org/10.1038/s41598-024-75695-5Download citationReceived: 26 February 2024Accepted: 08 October 2024Published: 16 October 2024DOI: https://doi.org/10.1038/s41598-024-75695-5Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

科学报告1424227（2024）。https://doi.org/10.1038/s41598-024-75695-5Download引文收到日期：2024年2月26日接受日期：2024年10月8日发布日期：2024年10月16日OI：https://doi.org/10.1038/s41598-024-75695-5Share本文与您共享以下链接的任何人都可以阅读此内容：获取可共享链接对不起，本文目前没有可共享的链接。复制到剪贴板。

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KeywordsBroilersAntioxidant indicatorsInflammatory responseGut microfloraOrganic trace mineralsMetabolic profile

关键词油脂抗氧化指标炎症反应微生物群落有机痕量矿物质代谢谱