Assessing the effects of a mixed Eimeria spp. challenge on performance, intestinal integrity, and the gut microbiome of broiler chickens

A mixed Eimeria spp. challenge model was designed to assess the effects of challenge on broiler chicken performance, intestinal integrity, and the gut microbiome for future use to evaluate alternative strategies for controlling coccidiosis in broiler chickens. The experimental design involved broiler chickens divided into two groups: a control group (uninfected) and a positive control group, infected with Eimeria acervulina (EA), Eimeria maxima (EM), and Eimeria tenella (ET). At day-of-hatch, 240 off-sex male broiler chicks were randomized and allocated to one of two treatment groups. The treatment groups included: (1) Non-challenged (NC, n = 5 replicate pens); and (2) challenged control (PC, n = 7 replicate pens) with 20 chickens/pen. Pen weights were recorded at d0, d16, d31, d42, and d52 to determine average body weight (BW) and (BWG). Feed intake was measured at d16, d31, d42, and d52 to calculate feed conversion ratio (FCR). Four diet phases included a starter d0–16, grower d16–31, finisher d31–42, and withdrawal d42–52 diet. At d18, chickens were orally challenged with 200 EA, 3,000 EM, and 500 ET sporulated oocysts/chicken. At d24 (6-day post-challenge) and d37 (19-day post-challenge), intestinal lesion scores were recorded. Additionally, at d24, FITC-d was used as a biomarker to evaluate intestinal permeability and ileal tissue sections were collected for histopathology and gene expression of tight junction proteins. Ileal and cecal contents were also collected to assess the impact of challenge on the microbiome. BWG and FCR from d16–31 was significantly (p < 0.05) reduced in PC compared to NC. At d24, intestinal lesion scores were markedly higher in the PC compared to the NC. Intestinal permeability was significantly increased in the PC group based on serum FITC-d levels. Cadherin 1 (CDH1), calprotectin (CALPR), and connexin 45 (Cx45) expression was also upregulated in the ileum of the PC group at d24 (6-day post-challenge) while villin 1 (VIL1) was downregulated in the ileum of the PC group. Additionally, Clostridium perfringens (ASV1) was enriched in the cecal content of the PC group. This model could be used to assess the effect of alternative coccidiosis control methods during the post-challenge with EA, EM, and ET.

[1]  Hongsheng Wang,et al.  Comprehensive analysis of gut microbiome and host transcriptome in chickens after Eimeria tenella infection , 2023, Frontiers in Cellular and Infection Microbiology.

[2]  I. Kyriazakis,et al.  The effects of arginine and branched-chain amino acid supplementation to reduced-protein diet on intestinal health, cecal short-chain fatty acid profiles, and immune response in broiler chickens challenged with Eimeria spp. , 2023, Poultry science.

[3]  H. Lillehoj,et al.  Effect of Dietary Organic Selenium on Growth Performance, Gut Health, and Coccidiosis Response in Broiler Chickens , 2023, Animals : an open access journal from MDPI.

[4]  A. Sattar,et al.  Biosynthesis and characterization of zinc oxide nanoparticles using Nigella sativa against coccidiosis in commercial poultry , 2023, Scientific reports.

[5]  W. Eisenreich,et al.  Effects of chronic stress and intestinal inflammation on commercial poultry health and performance: A review , 2023, German Journal of Veterinary Research.

[6]  M. Dkhil,et al.  In vivo anticoccidial, antioxidant, and anti-inflammatory activities of avocado fruit, Persea americana (Lauraceae), against Eimeria papillata infection. , 2023, Parasitology international.

[7]  Guanchen Liu,et al.  Effects of levels of methionine supplementations in forms of L- or DL-methionine on the performance, intestinal development, immune response, and antioxidant system in broilers challenged with Eimeria spp. , 2023, Poultry science.

[8]  C. Xue,et al.  Alginate Oligosaccharides Prevent Dextran-Sulfate-Sodium-Induced Ulcerative Colitis via Enhancing Intestinal Barrier Function and Modulating Gut Microbiota , 2023, Foods.

[9]  Jing Tang,et al.  Effect of riboflavin deficiency on intestinal morphology, jejunum mucosa proteomics, and cecal microbiota of Pekin ducks , 2022, Animal nutrition.

[10]  Liliana J. G. Silva,et al.  Coccidiostats and Poultry: A Comprehensive Review and Current Legislation , 2022, Foods.

[11]  Fan Yang,et al.  Compound probiotics alleviate cadmium-induced intestinal dysfunction and microbiota disorders in broilers. , 2022, Ecotoxicology and environmental safety.

[12]  M. Misiura,et al.  Quantifying the effect of coccidiosis on broiler performance and infection outcomes in the presence and absence of control methods , 2022, Poultry science.

[13]  S. López-Osorio,et al.  Chicken Coccidiosis: From the Parasite Lifecycle to Control of the Disease , 2021, Frontiers in Veterinary Science.

[14]  M. Adeleke,et al.  Understanding the interactions between Eimeria infection and gut microbiota, towards the control of chicken coccidiosis: a review , 2021, Parasite.

[15]  Annah Lee,et al.  Novel Models for Chronic Intestinal Inflammation in Chickens: Intestinal Inflammation Pattern and Biomarkers , 2021, Frontiers in Immunology.

[16]  N. Mabbott,et al.  Inside-out chicken enteroids with leukocyte component as a model to study host–pathogen interactions , 2021, Communications biology.

[17]  J. Rushton,et al.  Re-calculating the cost of coccidiosis in chickens , 2020, Veterinary Research.

[18]  N. Anthony,et al.  Intestinal Barrier Integrity in Heat-Stressed Modern Broilers and Their Ancestor Wild Jungle Fowl , 2020, Frontiers in Veterinary Science.

[19]  D. Spray,et al.  Gap and Tight Junctions in Liver , 2020 .

[20]  Adam Huczyński,et al.  Salinomycin and its derivatives - A new class of multiple-targeted "magic bullets". , 2019, European journal of medicinal chemistry.

[21]  William A. Walters,et al.  Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 , 2019, Nature Biotechnology.

[22]  M. Dhaenens,et al.  Host intestinal biomarker identification in a gut leakage model in broilers , 2019, Veterinary Research.

[23]  S. Dridi,et al.  Identification of Serum Biomarkers for Intestinal Integrity in a Broiler Chicken Malabsorption Model , 2019, Front. Vet. Sci..

[24]  S. Ricke,et al.  Evaluation of the Epithelial Barrier Function and Ileal Microbiome in an Established Necrotic Enteritis Challenge Model in Broiler Chickens , 2018, Front. Vet. Sci..

[25]  C. Li,et al.  Transgenic Eimeria tenella Expressing Profilin of Eimeria maxima Elicits Enhanced Protective Immunity and Alters Gut Microbiome of Chickens , 2018, Infection and Immunity.

[26]  H. Meng,et al.  Inheritance and Establishment of Gut Microbiota in Chickens , 2017, Front. Microbiol..

[27]  J. Latorre,et al.  Optimizing Fluorescein Isothiocyanate Dextran Measurement As a Biomarker in a 24-h Feed Restriction Model to Induce Gut Permeability in Broiler Chickens , 2017, Front. Vet. Sci..

[28]  Jose A Navas-Molina,et al.  Deblur Rapidly Resolves Single-Nucleotide Community Sequence Patterns , 2017, mSystems.

[29]  M. Dkhil,et al.  Profiling of jejunum inflammatory gene expression during murine eimeriosis. , 2017, Microbial pathogenesis.

[30]  T. Kumosani,et al.  A Review of Approaches Targeting the Replacement of Coccidiostat Application in Poultry Production , 2015 .

[31]  S. Hessenberger,et al.  Assessment of probiotics supplementation via feed or water on the growth performance, intestinal morphology and microflora of chickens after experimental infection with Eimeria acervulina, Eimeria maxima and Eimeria tenella , 2014, Avian pathology : journal of the W.V.P.A.

[32]  G. Wang,et al.  Quantitative Genetic Background of the Host Influences Gut Microbiomes in Chickens , 2013, Scientific Reports.

[33]  F. Wunderlich,et al.  Liver response of rabbits to Eimeria coecicola infections , 2012, Parasitology Research.

[34]  Thomas D. Schmittgen,et al.  Analyzing real-time PCR data by the comparative CT method , 2008, Nature Protocols.

[35]  G. Erf,et al.  Cell-mediated immunity in poultry. , 2004, Poultry science.

[36]  J. Barta,et al.  Analysis of immunological cross-protection and sensitivities to anticoccidial drugs among five geographical and temporal strains of Eimeria maxima. , 1997, International journal for parasitology.

[37]  J. Johnson,et al.  Anticoccidial drugs: lesion scoring techniques in battery and floor-pen experiments with chickens. , 1970, Experimental parasitology.

[38]  H. Woodrow,et al.  : A Review of the , 2018 .

[39]  C. Huttenhower,et al.  Microbial community function and biomarker discovery in the human microbiome , 2011, Genome Biology.