Effect of Glucose Oxidase and a Commercial Bacillus-based Direct Feed Microbial Supplementation on the Productive Performance, Intestinal IgA, Gut Permeability, and Cecal Microbiota of Broiler Chickens

Authors

    Rubén Merino-Guzmán * Departamento de Medicina y Zootecnia de Aves, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Mexico City, 04510, Mexico onirem@unam.mx
    Madeleine Luna-Cardoso Departamento de Medicina y Zootecnia de Aves, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Mexico City, 04510, Mexico
    Guillermo Tellez-Isaías Department of Poultry Science, University of Arkansas, Fayetteville, 72701, AR, USA
    Juan David Latorre Department of Poultry Science, University of Arkansas, Fayetteville, 72701, AR, USA
    Billy Marshall Hargis Department of Poultry Science, University of Arkansas, Fayetteville, 72701, AR, USA

Keywords:

Bacillus DFM, Glucose oxidase, Broiler chickens, Gut integrity, Microbiota, Intestinal IgA

Abstract

Restrictions on the use of antibiotic growth promoters in broiler chickens have stimulated the search for alternatives, such as probiotics and enzymes. Bacillus has benefits for intestinal microbial balance and productive performance; however, less is known about the effects of the enzyme glucose oxidase (GOx) in chickens, and there is scarce information about the combination of both additives on broiler performance and cecal microbiota. Chickens supplemented with either Bacillus (106 spores/g feed), GOx (100 U/kg feed), the combination of both, or a control group were evaluated. Improvements were observed in performance parameters and gut health, with a reduction in intestinal IgA concentration in the treated groups; however, no difference was noted in gut permeability (serum FITC-d concentration). Bacillus and GOx alone increased the cecum microbial Alpha diversity; meanwhile, the Beta diversity from the Bacillus group was different from that of the control and Bacillus-GOx groups. A reduction in harmful bacteria (Proteobacteria) along with an increase in beneficial bacteria (Firmicutes and Actinobacteria) was observed in the cecal microbiota composition from the treated groups. GOx treatment increased the phylum Actinobacteria. Bacillus and GOx can enhance the gut health of chickens by modulating the gut microbiota. However, no synergic effect was seen in the group receiving the additive combination. Further research is needed to more effectively demonstrate the effect.

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Author Biography

  • Rubén Merino-Guzmán, Departamento de Medicina y Zootecnia de Aves, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Mexico City, 04510, Mexico

    Full time Professor

References

Li C, Cai H, Li S, Liu G, Deng X, Bryden WL, et al. Comparing the potential of Bacillus amyloliquefaciens CGMCC18230 with antimicrobial growth promoters for growth performance, bone development, expression of phosphorus transporters, and excreta microbiome in broiler chickens. Poultry Science. 2022;101(11):102126.[PMID: 36099660] [PMCID: PMC9474562] [DOI]

Aslam B, Khurshid M, Arshad MI, Muzammil S, Rasool M, Yasmeen N, et al. Antibiotic Resistance: One Health One World Outlook. Front Cell Infect Microbiol. 2021;11:771510.[PMID: 34900756] [PMCID: PMC8656695] [DOI]

Wu S, Chen X, Li T, Ren H, Zheng L, Yang X. Changes in the gut microbiota mediate the differential regulatory effects of two glucose oxidases produced by Aspergillus niger and Penicillium amagasakiense on the meat quality and growth performance of broilers. Journal of Animal Science and Biotechnology. 2020;11(1):73.[PMID: 32647570] [PMCID: PMC7336442] [DOI]

Muniyappan M, Chen N, Liu Y, Kim IH. The Effect of Dietary Glucose Oxidase Supplementation on Production Performance, Egg Quality and Nutrient Digestibility in Laying Hens. Brazilian Journal of Poultry Science. 2022;24[DOI]

Qu W, Liu J. Effects of glucose oxidase supplementation on the growth performance, antioxidative and inflammatory status, gut function, and microbiota composition of broilers fed moldy corn. Frontiers in Physiology. 2021;12:646393.[PMID: 34220529] [PMCID: PMC8244819] [DOI]

Bauer JA, Zámocká M, Majtán J, Bauerová-Hlinková V. Glucose oxidase, an enzyme “Ferrari”: Its structure, function, production and properties in the light of various industrial and biotechnological applications. Biomolecules. 2022;12(3):472.[PMID: 35327664] [PMCID: PMC8946809] [DOI]

Khan S, Moore RJ, Stanley D, Chousalkar KK. The gut microbiota of laying hens and its manipulation with prebiotics and probiotics to enhance gut health and food safety. Applied and Environmental Microbiology. 2020;86(13):e00600-20.[PMID: 32332137] [PMCID: PMC7301851] [DOI]

Popov IV, Algburi A, Prazdnova EV, Mazanko MS, Elisashvili V, Bren AB, et al. A review of the effects and production of spore-forming probiotics for poultry. Animals. 2021;11(7):1941.[PMID: 34209794] [PMCID: PMC8300232] [DOI]

Hernandez-Patlan D, Solis-Cruz B, Latorre JD, Merino-Guzman R, Morales Rodríguez M, Ausland C, et al. Whole-genome sequence and interaction analysis in the production of six enzymes from the three Bacillus strains present in a commercial direct-fed microbial (NorumTM) using a Bliss Independence test. Frontiers in Veterinary Science. 2022;9:784387.[PMID: 35274019] [PMCID: PMC8902298] [DOI]

Wang W, Xie R, Cao Q, Ye H, Zhang C, Dong Z, et al. Effects of glucose oxidase on growth performance, clinical symptoms, serum parameters, and intestinal health in piglets challenged by enterotoxigenic Escherichia coli. Frontiers in Microbiology. 2022;13:994151.[PMID: 36267185] [PMCID: PMC9578003] [DOI]

Wang Y, Wang B, Zhan X, Wang Y, Li W. Effects of glucose oxidase and its combination with B. amyloliquefaciens SC06 on intestinal microbiota, immune response and antioxidative capacity in broilers. Animal. 2022;16(3):100473.[PMID: 35218993] [DOI]

Gao S, Zhang L, Zhu D, Huang J, Yang J, Jiang J, et al. Effects of glucose oxidase and Bacillus subtilis on growth performance and serum biochemical indices of broilers exposed to aflatoxin B1 and endotoxin. Animal Feed Science and Technology. 2022;286:115186[DOI]

Adhikari B, Hernandez-Patlan D, Solis-Cruz B, Kwon YM, Arreguin MA, Latorre JD, et al. Evaluation of the antimicrobial and anti-inflammatory properties of Bacillus-DFM (NorumTM) in broiler chickens infected with Salmonella Enteritidis. Frontiers in Veterinary Science. 2019;6:282.[PMID: 31508436] [PMCID: PMC6718558] [DOI]

Cobb V. Cobb500 Broiler Performance & Nutrition Supplement. Siloam Springs: Cobb-Vantress Inc.; 2022.

Baxter MF, Merino-Guzman R, Latorre JD, Mahaffey BD, Yang Y, Teague KD, et al. Optimizing fluorescein isothiocyanate dextran measurement as a biomarker in a 24-h feed restriction model to induce gut permeability in broiler chickens. Frontiers in Veterinary Science. 2017;4:56.[PMID: 28470003] [PMCID: PMC5396023] [DOI]

Merino-Guzmán R, Latorre JD, Delgado R, Hernandez-Velasco X, Wolfenden AD, Teague KD, et al. Comparison of total immunoglobulin A levels in different samples in Leghorn and broiler chickens. Asian Pacific Journal of Tropical Biomedicine. 2017;7(2):116-20[DOI]

Kogut MH, Lee A, Santin E. Microbiome and pathogen interaction with the immune system. Poultry Science. 2020;99(4):1906-13.[PMID: 32241470] [PMCID: PMC7587753] [DOI]

Maguey-González JA, Liu J, Zhang G, Latorre JD, Hernández-Ramírez JO, de Jesús Nava-Ramírez M, et al. Assessment of the impact of humic acids on intestinal microbiota, gut integrity, ileum morphometry, and cellular immunity of turkey poults fed an aflatoxin B1-contaminated diet. Toxins. 2024;16(3):122.[PMID: 38535788] [PMCID: PMC10975313] [DOI]

Qin B, Xia Y, Wang S, Du X. A novel Bayesian classification for uncertain data. Knowledge-Based Systems. 2011;24(8):1151-8[DOI]

Littell RC, Stroup WW, Freund RJ. SAS for Linear Models. Nashville, TN: John Wiley & Sons; 2002.

Paulson JN, Stine OC, Bravo HC, Pop M. Differential abundance analysis for microbial marker-gene surveys. Nature Methods. 2013;10(12):1200-2.[PMID: 24076764] [PMCID: PMC4010126] [DOI]

Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology. 2014;15(12):550.[PMID: 25516281] [PMCID: PMC4302049] [DOI]

Rivera-Pérez W, Barquero-Calvo E, Chaves AJ. Effect of the use of probiotic Bacillus subtilis (QST 713) as a growth promoter in broilers: An alternative to bacitracin methylene disalicylate. Poultry Science. 2021;100(9):101372.[PMID: 32316269] [PMCID: PMC7222747] [DOI]

Saleh AA, Paray BA, Dawood MAO. Olive cake meal and Bacillus licheniformis impacted the growth performance, muscle fatty acid content, and health status of broiler chickens. Animals. 2020;10(4):695[DOI]

Zhao Y, Li P, Chen N, Liu Y, Liu D, Guo Y. Effects of housing systems and glucose oxidase on growth performance and intestinal health of Beijing You Chickens. Poultry Science. 2021;100(4):100943.[PMID: 33652241] [PMCID: PMC7921002] [DOI]

Meng Y, Huo H, Zhang Y, Bai S, Wang R, Zhang K, et al. Effects of dietary glucose oxidase supplementation on the performance, apparent ileal amino acids digestibility, and ileal microbiota of broiler chickens. Animals. 2021;11(10):2909.[PMID: 34679930] [PMCID: PMC8532941] [DOI]

Wu S, Li T, Niu H, Zhu Y, Liu Y, Duan Y, et al. Effects of glucose oxidase on growth performance, gut function, and cecal microbiota of broiler chickens. Poultry Science. 2019;98(2):828-41.[PMID: 30169708] [DOI]

Wang Y, Wang Y, Xu H, Mei X, Gong L, Wang B, et al. Direct-fed glucose oxidase and its combination with B. amyloliquefaciens SC06 on growth performance, meat quality, intestinal barrier, antioxidative status, and immunity of yellow-feathered broilers. Poultry Science. 2018;97(10):3540-9.[PMID: 30085304] [DOI]

Stanley D, Hughes RJ, Moore RJ. Microbiota of the chicken gastrointestinal tract: Influence on health, productivity and disease. Applied Microbiology and Biotechnology. 2014;98(10):4301-10.[PMID: 24643736] [DOI]

Oakley BB, Lillehoj HS, Kogut MH, Kim WK, Maurer JJ, Pedroso A, et al. The chicken gastrointestinal microbiome. FEMS Microbiology Letters. 2014;360(2):100-12[PMCID: 25263745] [DOI]

Madden JAJ, Hunter JO. A review of the role of the gut microflora in irritable bowel syndrome and the effects of probiotics. British Journal of Nutrition. 2002;88(S1):S67-S72.[PMID: 12215182] [DOI]

Zhao Y, Fu J, Li P, Chen N, Liu Y, Liu D, et al. Effects of dietary glucose oxidase on growth performance and intestinal health of AA broilers challenged by Clostridium perfringens. Poultry Science. 2022;101(1):101553.[PMID: 34852314] [PMCID: PMC8639461] [DOI]

Ranjitkar S, Lawley B, Tannock G, Engberg RM. Bacterial succession in the broiler gastrointestinal tract. Applied and Environmental Microbiology. 2016;82(8):2399-410.[PMID: 26873323] [PMCID: PMC4959490] [DOI]

Shin NR, Whon TW, Bae JW. Proteobacteria: Microbial signature of dysbiosis in gut microbiota. Trends in Biotechnology. 2015;33(9):496-503.[PMID: 26210164] [DOI]

Al-Shaibani MM, Radin Mohamed RMS, Sidik NM, Enshasy HAE, Al-Gheethi A, Noman E, et al. Biodiversity of secondary metabolites compounds isolated from phylum Actinobacteria and its therapeutic applications. Molecules. 2021;26(15):4504.[PMID: 34361657] [PMCID: PMC8347454] [DOI]

Huang S, Chen J, Cui Z, Ma K, Wu D, Luo J, et al. Lachnospiraceae-derived butyrate mediates protection of high fermentable fiber against placental inflammation in gestational diabetes mellitus. Science Advances. 2023;9(44):eadi7337.[PMID: 37922350] [PMCID: PMC10624355] [DOI]

Barekatain R, Chrystal PV, Nowland T, Moss AF, Howarth GS, Van TTH, et al. Negative consequences of reduced protein diets supplemented with synthetic amino acids for performance, intestinal barrier function, and caecal microbiota composition of broiler chickens. Animal Nutrition. 2023;13:216-28.[PMID: 37388459] [PMCID: PMC10300400] [DOI]

Azad MAK, Sarker M, Li T, Yin J. Probiotic species in the modulation of gut microbiota: An overview. BioMed Research International. 2018;2018:9478630.[PMID: 29854813] [PMCID: PMC5964481] [DOI]

Bilal M, Achard C, Barbe F, Chevaux E, Ronholm J, Zhao X. Bacillus pumilus and Bacillus subtilis promote early maturation of cecal microbiota in broiler chickens. Microorganisms. 2021;9(9):1899.[PMID: 34576794] [PMCID: PMC8465073] [DOI]

Shi L, Li Y, Liu Y, Jia H. Alterations of gut microbiota and cytokines in elevated serum diamine oxidase disorder. Medicine. 2022;101(50):e31966.[PMID: 36550793] [PMCID: PMC9771309] [DOI]

Diaz Carrasco JM, Casanova NA, Fernández Miyakawa ME. Microbiota, gut health and chicken productivity: What is the connection? Microorganisms. 2019;7(10):374.[PMID: 31547108] [PMCID: PMC6843312] [DOI]

Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proceedings of the National Academy of Sciences. 2008;105(43):16731-6.[PMID: 18936492] [PMCID: PMC2575488] [DOI]

Richards P, Fothergill J, Bernardeau M, Wigley P. Development of the caecal microbiota in three broiler breeds. Frontiers in Veterinary Science. 2019;6:201.[PMID: 31294039] [PMCID: PMC6603203] [DOI]

Chasser K, McGovern K, Duff A, Graham B, Briggs W, Rodrigues D, et al. Evaluation of day of hatch exposure to various Enterobacteriaceae on inducing gastrointestinal inflammation in chicks through two weeks of age. Poultry Science. 2021;100(7):101193.[PMID: 34087698] [PMCID: PMC8182431] [DOI]

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Published

2025-10-01

Submitted

2025-07-03

Revised

2025-08-01

Accepted

2025-08-04

How to Cite

Merino-Guzman, R., Madeleine Luna-Cardoso, M. L.-C., Tellez-Isaías, G. ., Latorre, J. D. ., & Marshall Hargis, B. . (2025). Effect of Glucose Oxidase and a Commercial Bacillus-based Direct Feed Microbial Supplementation on the Productive Performance, Intestinal IgA, Gut Permeability, and Cecal Microbiota of Broiler Chickens. Journal of Poultry Sciences and Avian Diseases, 3(4), 1-11. https://jpsad.com/index.php/jpsad/article/view/148

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