{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:32:44Z","timestamp":1787027564105,"version":"build-2736575974"},"reference-count":51,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,4,26]],"date-time":"2022-04-26T00:00:00Z","timestamp":1650931200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Department of Agriculture, Environment and Rural Affairs for Northern Ireland","award":["123"],"award-info":[{"award-number":["123"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Poultry farming is growing globally, particularly in developing countries, to meet the demands of growing populations for poultry meat and eggs. This is likely to lead to an increase in the use of antibiotics in poultry feed, thus contributing to the development and spread of antibiotic resistance which, poses a serious threat to human and animal health worldwide. One way of reducing this threat is to reduce the use of antibiotics in poultry production by finding effective and sustainable antibiotic alternatives that can be used to support poultry health and productivity. Therefore, this study evaluates the incorporation of three medicinal plants, Anemone chinensis Bunge, Smilax glabra Roxb, and Agrimonia pilosa Ledeb, in poultry feed on production performance, nutrient digestibility, and bacteria in the chicken caecum in a 35-day performance trial with 420-day-old male Ross 308 broilers. Groups of randomly selected chicks received one of six dietary treatments. These included five experimental diets of reduced nutrient specifications as a negative control (NC); with amoxicillin as a positive antibiotic control (PC1); with A. pilosa Ledeb (NC1); with A. chinensis Bunge (NC2); and with S. glabra Roxb (NC3). One other positive control diet contained the recommended nutrient specification (PC2). Weight gain and feed intake were measured weekly and used to calculate the feed conversion ratio as performance parameters. Bacteria were enumerated from chicken caecum using a traditional plating method and selective agar. S. glabra Roxb and A. chinensis Bunge showed comparable effects to amoxicillin with significantly increased weight gain in birds offered these diets, compared to those offered the negative control from days 0 to 35 (p &lt; 0.001). S. glabra Roxb exhibited effects similar to the amoxicillin control group with an improved feed conversion ratio (p &lt; 0.001). In addition, S. glabra Roxb decreased numbers of E. coli and Campylobacter spp. on days 21 (p &lt; 0.05) and 35 (p &lt; 0.01) and increased numbers of lactic acid bacteria comparable to the antibiotic group on days 14 (p &lt; 0.001) and 35 (p &lt; 0.01). The findings of this in vivo trial highlight the potential of S. glabra Roxb and A. chinensis Bunge as beneficial feed material to promote poultry health and productivity in the absence of antibiotics.<\/jats:p>","DOI":"10.3390\/ani12091110","type":"journal-article","created":{"date-parts":[[2022,4,26]],"date-time":"2022-04-26T11:45:55Z","timestamp":1650973555000},"page":"1110","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["The Effects of Agrimonia pilosa Ledeb, Anemone chinensis Bunge, and Smilax glabra Roxb on Broiler Performance, Nutrient Digestibility, and Gastrointestinal Tract Microorganisms"],"prefix":"10.3390","volume":"12","author":[{"given":"Rebekah L.","family":"McMurray","sequence":"first","affiliation":[{"name":"School of Biological Sciences, Queen\u2019s University Belfast, Belfast BT9 5DL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M. Elizabeth E.","family":"Ball","sequence":"additional","affiliation":[{"name":"Livestock Production Sciences Branch, Agri-Food and Biosciences Institute, Hillsborough BT26 6DR, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Linton","sequence":"additional","affiliation":[{"name":"Bacteriology Branch Agri-Food and Biosciences Institute, Belfast BT9 5PX, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurette","family":"Pinkerton","sequence":"additional","affiliation":[{"name":"Bacteriology Branch Agri-Food and Biosciences Institute, Belfast BT9 5PX, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carmel","family":"Kelly","sequence":"additional","affiliation":[{"name":"Bacteriology Branch Agri-Food and Biosciences Institute, Belfast BT9 5PX, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan","family":"Lester","sequence":"additional","affiliation":[{"name":"Devenish Nutrition, Belfast BT1 3BG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline","family":"Donaldson","sequence":"additional","affiliation":[{"name":"Devenish Nutrition, Belfast BT1 3BG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1171-2623","authenticated-orcid":false,"given":"Igori","family":"Balta","sequence":"additional","affiliation":[{"name":"Bacteriology Branch Agri-Food and Biosciences Institute, Belfast BT9 5PX, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael M.","family":"Tunney","sequence":"additional","affiliation":[{"name":"School of Pharmacy, Queen\u2019s University Belfast, Belfast BT9 7BL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3011-3108","authenticated-orcid":false,"given":"Nicolae","family":"Corcionivoschi","sequence":"additional","affiliation":[{"name":"Bacteriology Branch Agri-Food and Biosciences Institute, Belfast BT9 5PX, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chen","family":"Situ","sequence":"additional","affiliation":[{"name":"Institute for Global Food Security, Queen\u2019s University Belfast, Belfast BT9 5DL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,4,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1017\/S0043933917000071","article-title":"Global poultry production: Current state and future outlook and challenges","volume":"73","author":"Mottet","year":"2017","journal-title":"World\u2019s Poult. Sci. J."},{"key":"ref_2","unstructured":"Alexandratos, N., and Bruinsma, J. (2012). World agriculture towards 2030\/2050. Food Agric. Organ. U. N., 1\u2013147."},{"key":"ref_3","unstructured":"(2022, April 04). OECD-FAO Agricultural Outlook 2020\u20132029. Available online: https:\/\/www.oecd-ilibrary.org\/agriculture-and-food\/oecd-fao-agricultural-outlook-2020-2029_1112c23b-en."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"5649","DOI":"10.1073\/pnas.1503141112","article-title":"Global trends in antimicrobial use in food animals","volume":"112","author":"Brower","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_5","unstructured":"OIE (2018). Annual Report on Antimicrobial Agents Intended for Use in Animals, OIE."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/S0924-8579(02)00394-1","article-title":"The use and resistance to antibiotics in the community","volume":"21","year":"2003","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1016\/S1473-3099(11)70054-8","article-title":"Non-prescription antimicrobial use worldwide: A systematic review","volume":"11","author":"Morgan","year":"2011","journal-title":"Lancet Infect. Dis."},{"key":"ref_8","unstructured":"O\u2019Neill, J. (2016). Tackling Drug-Resistant Infections Globally: Final Report and Recommendations, Wellcome Trust and HM Government."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1111\/1541-4337.12387","article-title":"Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: A comprehensive review","volume":"17","author":"Olaimat","year":"2018","journal-title":"Compr. Rev. Food Sci. Food Saf."},{"key":"ref_10","unstructured":"World Health Organisation (2015). WHO Estimates of the Global Burden of Foodborne Diseases, World Health Organisation."},{"key":"ref_11","unstructured":"Interagency Coordination Group on Antimicrobial Resistance (2022, April 04). No Time to Wait: Securing the Future from Drug Resistant Infections. Available online: https:\/\/www.who.int\/docs\/default-source\/documents\/no-time-to-wait-securing-the-future-from-drug-resistant-infections-en.pdf."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1186\/s13567-018-0562-6","article-title":"Phytochemicals as antibiotic alternatives to promote growth and enhance host health","volume":"49","author":"Lillehoj","year":"2018","journal-title":"Vet. Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2295","DOI":"10.3923\/javaa.2010.2295.2304","article-title":"Phytogenics as new class of feed additive in poultry industry","volume":"9","author":"Hashemi","year":"2010","journal-title":"J. Anim. Vet. Adv."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2123","DOI":"10.1016\/S2095-3119(19)62566-9","article-title":"Effects of dietary graded levels of cinnamon essential oil and its combination with bamboo leaf flavonoid on immune function, antioxidative ability and intestinal microbiota of broilers","volume":"18","author":"Yang","year":"2019","journal-title":"J. Integr. Agric."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1017\/S1466252316000207","article-title":"Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: A review","volume":"18","author":"Gadde","year":"2017","journal-title":"Anim. Health Res. Rev."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"McMurray, R.L., Ball, M.E.E., Tunney, M.M., Corcionivoschi, N., and Situ, C. (2020). Antibacterial activity of four plant extracts extracted from traditional Chinese medicinal plants against Listeria monocytogenes, Escherichia coli, and Salmonella enterica subsp. enterica serovar Enteritidis. Microorganisms, 8.","DOI":"10.3390\/microorganisms8060962"},{"key":"ref_17","unstructured":"(2020, April 16). Bioline Bioline. Available online: https:\/\/www.bioline.com\/uk\/downloads\/dl\/file\/id\/2697\/mytaq_red_mix_product_manual.pdf."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1080\/10408398.2014.935847","article-title":"Control of Campylobacter in Poultry Industry from Farm to Poultry Processing Unit: A Review","volume":"57","author":"Umaraw","year":"2017","journal-title":"Crit. Rev. Food Sci. Nutr."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Davis, G.S., Waits, K., Nordstrom, L., Grande, H., Weaver, B., Papp, K., Horwinski, J., Koch, B., Hungate, B.A., and Liu, C.M. (2018). Antibiotic-resistant Escherichia coli from retail poultry meat with different antibiotic use claims. BMC Microbiol., 18.","DOI":"10.1186\/s12866-018-1322-5"},{"key":"ref_20","unstructured":"(2020, January 24). The Plant List. Available online: http:\/\/www.theplantlist.org\/."},{"key":"ref_21","unstructured":"Clinical and Laboratory Standards Institute (2009). Methods for Dilution: Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically, Approved Standard, Clinical and Laboratory Standards Institute. [8th ed.]."},{"key":"ref_22","unstructured":"Aviagen (2018). Broiler Management Handbook 2018, Aviagen."},{"key":"ref_23","unstructured":"Aviagen (2019). Ross 308 Broiler: Nutrition Specifications, Aviagen."},{"key":"ref_24","first-page":"6177","article-title":"Effect of dietary oregano (Origanum vulgare L.) essential oil on growth performance, cecal microflora and serum antioxidant activity of broiler chickens","volume":"10","author":"Roofchaee","year":"2011","journal-title":"Afr. J. Biotechnol."},{"key":"ref_25","unstructured":"AOAC (1998). Official Method 934.01 Loss on Drying (Moisture) at 95\u2013100 \u00b0C for Feeds Dry Matter on Oven Drying at 95\u2013100 \u00b0C for Feeds First, AOAC."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2110","DOI":"10.3382\/ps\/pew485","article-title":"Effects of dietary coarsely ground corn and 3 bedding floor types on broiler live performance, litter characteristics, gizzard and proventriculus weight, and nutrient digestibility","volume":"96","author":"Xu","year":"2017","journal-title":"Poult. Sci."},{"key":"ref_27","first-page":"184","article-title":"Comparing the effects of a combined phytogenic feed additive with an individual essential oil of oregano on intestinal morphology and microflora in broilers","volume":"46","year":"2017","journal-title":"J. Appl. Anim. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1391","DOI":"10.3382\/ps\/pex413","article-title":"TYPLEX\u00ae Chelate, a novel feed additive, inhibits Campylobacter jejuni biofilm formation and cecal colonization in broiler chickens","volume":"97","author":"Khattak","year":"2018","journal-title":"Poult. Sci."},{"key":"ref_29","unstructured":"AOAC (2019). Official Methods of Analysis, AOAC. [21st ed.]."},{"key":"ref_30","first-page":"535","article-title":"Collaborative study of the quantitative determination of titanium dioxide in cheese","volume":"56","author":"Leone","year":"1973","journal-title":"Assoc. Off. Anal. Chem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1017\/S002185960005526X","article-title":"The use of titanium dioxide for determining apparent nutrient digestibility in mature domestic fowls (Gallus domesticus)","volume":"99","author":"Peddie","year":"1982","journal-title":"J. Agric. Sci."},{"key":"ref_32","unstructured":"European Commission Commission regulation (EC) (2009). No 152\/2009 of 27 January 2009 laying down the methods of sampling and analysis for the official control of feed. Off. J. Eur. Union, 54, 1\u2013130."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"02662","DOI":"10.3389\/fmicb.2019.02662","article-title":"Dietary supplementation with citrus extract altered the intestinal microbiota and microbial metabolite profiles and enhanced the mucosal immune homeostasis in yellow-feathered broilers","volume":"10","author":"Yu","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"471","DOI":"10.3382\/japr.2008-00023","article-title":"Effect of dietary mannan oligosaccharide from bio-mos or SAF-mannan on live performance of broiler chickens","volume":"17","author":"Benites","year":"2008","journal-title":"J. Appl. Poult. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1093\/ps\/79.11.1557","article-title":"Characterization of the contribution of water activity and moisture content to the population distribution of Salmonella spp. in commercial poultry houses","volume":"79","author":"Hayes","year":"2000","journal-title":"Poult. Sci."},{"key":"ref_36","unstructured":"Darambazar, E. (2019). Determination of titanium dioxide as a livestock digestibility marker. Assay Protocol. Univ. Sask., 10."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.3382\/ps\/pew388","article-title":"Effect of elevated dietary amino acid levels in high canola meal diets on productive traits and cecal microbiota population of broiler chickens in a pair-feeding study","volume":"96","author":"Toghyani","year":"2017","journal-title":"Poult. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"362","DOI":"10.4314\/sajas.v45i4.2","article-title":"Intestinal morphology, digestive organ size and digesta pH of broiler chickens fed diets supplemented with or without Moringa oleifera leaf meal","volume":"45","author":"Nkukwana","year":"2015","journal-title":"S. Afr. J. Anim. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1590\/1516-635X1704419-426","article-title":"Effects of coriander essential oil on the performance, blood characteristics, intestinal microbiota and histological of broilers","volume":"17","author":"Ghazanfari","year":"2015","journal-title":"Braz. J. Poult. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"272","DOI":"10.3382\/ps.2012-02603","article-title":"Influence of penicillin on microbial diversity of the cecal microbiota in broiler chickens","volume":"92","author":"Singh","year":"2013","journal-title":"Poult. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Maki, J.J., Klima, C.L., Sylte, M.J., and Looft, T. (2019). The microbial pecking order: Utilization of intestinal microbiota for poultry health. Microorganisms, 7.","DOI":"10.3390\/microorganisms7100376"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1111\/j.1574-6941.2002.tb00978.x","article-title":"Molecular analysis of bacterial populations in the ileum of broiler chickens and comparison with bacteria in the cecum","volume":"41","author":"Gong","year":"2002","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_43","first-page":"1","article-title":"Applications of Probiotics in Poultry: Enhancing Immunity and Beneficial Effects on Production Performances and Health\u2014A Review","volume":"13","author":"Dhama","year":"2011","journal-title":"J. Immunol. Immunopathol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Danzeisen, J.L., Kim, H.B., Isaacson, R.E., Tu, Z.J., and Johnson, T.J. (2011). Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0027949"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1099\/mic.0.000597","article-title":"Increased productivity in poultry birds by sub-lethal dose of antibiotics is arbitrated by selective enrichment of gut microbiota, particularly short-chain fatty acid producers","volume":"164","author":"Banerjee","year":"2018","journal-title":"Microbiology"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"658","DOI":"10.3906\/vet-1803-53","article-title":"The effect of using rosemary (Rosmarinus officinalis) in broiler nutrition on production parameters, slaughter characteristics, and gut microbiological population","volume":"42","author":"Rakonjac","year":"2018","journal-title":"Turk. J. Vet. Anim. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"237","DOI":"10.3382\/japr.2010-00181","article-title":"Antibacterial effect of trans-cinnamaldehyde, eugenol, carvacrol, and thymol on Salmonella enteritidis and Campylobacter jejuni in chicken cecal contents in vitro","volume":"19","author":"Johny","year":"2010","journal-title":"J. Appl. Poult. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"448","DOI":"10.4081\/ijas.2015.3930","article-title":"Effect of different dietary levels of rosemary (Rosmarinus officinalis) and yarrow (Achillea millefolium) on the growth performance, carcass traits and ileal microbiota of broilers","volume":"14","author":"Norouzi","year":"2015","journal-title":"Ital. J. Anim. Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.jep.2018.12.046","article-title":"Gentiana scabra Bunge roots alleviates skin lesions of contact dermatitis in mice","volume":"233","author":"Yang","year":"2019","journal-title":"J. Ethnopharmacol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1111\/jpn.12256","article-title":"Correlations between changes in intestinal microbiota composition and performance parameters in broiler chickens","volume":"99","author":"Rubio","year":"2015","journal-title":"J. Anim. Physiol. Anim. Nutr."},{"key":"ref_51","first-page":"501","article-title":"Effect of crude fibre, feeding level and body weight on apparent digestibility of compound feeds by swine","volume":"34","author":"Everts","year":"1986","journal-title":"Neth. J. Agric. Sci."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/12\/9\/1110\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:01:09Z","timestamp":1760137269000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/12\/9\/1110"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,26]]},"references-count":51,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["ani12091110"],"URL":"https:\/\/doi.org\/10.3390\/ani12091110","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,26]]}}}