{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,12]],"date-time":"2025-12-12T13:43:19Z","timestamp":1765546999482,"version":"build-2065373602"},"reference-count":49,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,1,6]],"date-time":"2023-01-06T00:00:00Z","timestamp":1672963200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Mexican Council of Science and Technology (CONACYT)","award":["PDCPN_2017_4777","IA101253","2019-69012-29905","2019-69012-29905"],"award-info":[{"award-number":["PDCPN_2017_4777","IA101253","2019-69012-29905","2019-69012-29905"]}]},{"name":"USDA-NIFA Sustainable Agriculture Systems","award":["PDCPN_2017_4777","IA101253","2019-69012-29905","2019-69012-29905"],"award-info":[{"award-number":["PDCPN_2017_4777","IA101253","2019-69012-29905","2019-69012-29905"]}]},{"name":"Empowering US Broiler Production for Transformation and Sustainability USDA-NIFA (Sustainable Agriculture Systems)","award":["PDCPN_2017_4777","IA101253","2019-69012-29905","2019-69012-29905"],"award-info":[{"award-number":["PDCPN_2017_4777","IA101253","2019-69012-29905","2019-69012-29905"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>The mechanisms of action of humic substances (HS) as growth promoters in poultry are unknown. In this study, the productive performance, histology, and number of goblet cells (GC) in the intestinal villi of broilers under steady-state digestive conditions and under abrupt changes in diet with the addition of HS was evaluated. Broilers housed individually were offered three treatments from 14\u201328 days: 1 = diet with white corn\/soybean meal, without growth promoter antibiotics (nonGPA); 2 = with GPA (GPA); and 3 = with 0.3% HS. At day 28, two diets were suddenly introduced: (A) white corn\/soybean meal plus dried distillers\u2019 grains with solubles (DDGS); and (B) white\/blue corn\/soybean meal\/DDGS, keeping the three original treatments. Diets A and B were also exchanged on day 37. FCR was lower with GPA and HS compared to nonGPA from 14\u201338 days (p &lt; 0.05); at day 28, under steady-state digestive conditions, HS had a similar effect to GPA on the histology and GC number in the jejunum villi. The number of GC in the jejunum of HS-fed broilers on days 29 and 38, after diet changes, behaves similarly to that of AGP-fed broilers (p &gt; 0.05). HS appears to strengthen the mucosal protection of the epithelium of the intestine.<\/jats:p>","DOI":"10.3390\/ani13020212","type":"journal-article","created":{"date-parts":[[2023,1,9]],"date-time":"2023-01-09T03:25:58Z","timestamp":1673234758000},"page":"212","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Effect of the Addition of Humic Substances on Morphometric Analysis and Number of Goblet Cells in the Intestinal Mucosa of Broiler Chickens"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0154-1012","authenticated-orcid":false,"given":"Yair Rom\u00e1n","family":"L\u00f3pez-Garc\u00eda","sequence":"first","affiliation":[{"name":"Posgrado en Ciencias de la Producci\u00f3n y de la Salud Animal, Facultad de Estudios Superiores Cuautitl\u00e1n, Universidad Nacional Aut\u00f3noma de M\u00e9xico, Km 1 carretera a Col\u00f3n, Queretaro 76280, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0905-4959","authenticated-orcid":false,"given":"Sergio","family":"G\u00f3mez-Rosales","sequence":"additional","affiliation":[{"name":"Centro Nacional de Investigaci\u00f3n Disciplinaria en Fisiolog\u00eda y Mejoramiento Animal, INIFAP, Km 1 carretera a Col\u00f3n, Queretaro 76280, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mar\u00eda de Lourdes","family":"Angeles","sequence":"additional","affiliation":[{"name":"Centro Nacional de Investigaci\u00f3n Disciplinaria en Fisiolog\u00eda y Mejoramiento Animal, INIFAP, Km 1 carretera a Col\u00f3n, Queretaro 76280, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"H\u00e9ctor","family":"Jim\u00e9nez-Severiano","sequence":"additional","affiliation":[{"name":"Centro Nacional de Investigaci\u00f3n Disciplinaria en Fisiolog\u00eda y Mejoramiento Animal, INIFAP, Km 1 carretera a Col\u00f3n, Queretaro 76280, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5328-8808","authenticated-orcid":false,"given":"Rub\u00e9n","family":"Merino-Guzman","sequence":"additional","affiliation":[{"name":"Departamento de Medicina y Zootecnia de Aves, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Aut\u00f3noma de M\u00e9xico, Ciudad de Mexico 04510, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2416-2747","authenticated-orcid":false,"given":"Guillermo","family":"T\u00e9llez-Isaias","sequence":"additional","affiliation":[{"name":"Department of Poultry Science, University of Arkansas, Fayetteville, AR 72701, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"126","DOI":"10.3923\/pjn.2005.126.134","article-title":"Humic Acid Substances in Animal Agriculture","volume":"4","author":"Islam","year":"2005","journal-title":"Pakis. J. Nut."},{"key":"ref_2","first-page":"167","article-title":"Humic Acid as a Feed Additive in Poultry Diets: A Review","volume":"20","author":"Arif","year":"2019","journal-title":"Iran. J. Vet. Res."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.rvsc.2022.01.004","article-title":"Effects of humic acids on the recovery of different bacterial strains in an in vitro chicken digestive model","volume":"145","author":"Angeles","year":"2022","journal-title":"Res. Vet. Sci."},{"key":"ref_4","unstructured":"Abdelhadi, M. (2022). Mechanisms of Action of Humic Substances as Growth Promoters in Animals. Humus and Humic Substances\u2014Recent Advances, IntechOpen."},{"key":"ref_5","first-page":"663","article-title":"Influence of different levels of humic acid and esterified glucomannan on growth performance and intestinal morphology of broiler chickens","volume":"3","author":"Taklimi","year":"2012","journal-title":"Agric. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1002\/jsfa.4541","article-title":"Performance, carcass, gastrointestinal tract and meat quality traits, and selected blood parameters of broilers fed diets supplemented with humic substances","volume":"92","author":"Ozturk","year":"2012","journal-title":"J. Sci. Food. Agric."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"914","DOI":"10.4314\/sajas.v47i6.19","article-title":"Humic acid and enzymes in canola-based broiler diets: Effects on bone development, intestinal histomorphology and immune development","volume":"47","author":"Disetlhe","year":"2017","journal-title":"S. Afr. J. Anim. Sci."},{"key":"ref_8","first-page":"4","article-title":"Humins\u00e4urehaltige Tierarzneimittel in Therapie and Prophylaxe bei gastrointestinalen Erkrankungen von Hund und Katze","volume":"46","author":"Bartels","year":"1991","journal-title":"Mon. Vet."},{"key":"ref_9","unstructured":"EMEA (2022, October 29). Committee for Veterinary Medical Products. Humic Acids and Their Sodium Salts, Summary Report. Committee for Veterinary Medicinal Products., Available online: http:\/\/www.ema.europa.eu\/docs\/en_GB\/document_library\/Maximum_Residue_Limits_-_Report\/2009\/11\/WC500014416."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1002","DOI":"10.1111\/asj.13011","article-title":"Effect of Humic Acids on Intestinal Viscosity, Leaky Gut and Ammonia Excretion in a 24 h Feed Restriction Model to Induce Intestinal Permeability in Broiler Chickens","volume":"89","author":"Michel","year":"2018","journal-title":"Anim. Sci. J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1080\/09540105.2019.1707780","article-title":"The effect of humic substances on gut microbiota and immune response of broilers","volume":"31","year":"2020","journal-title":"Food Agric. Immunol."},{"key":"ref_12","first-page":"288","article-title":"Response of broiler chickens to varying dosage of humic acid in drinking water","volume":"29","author":"Lala","year":"2017","journal-title":"J. Anim. Prod. Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"745849","DOI":"10.3389\/fimmu.2021.745849","article-title":"Development and Functional Properties of Intestinal Mucus Layer in Poultry","volume":"12","author":"Duangnumsawang","year":"2021","journal-title":"Front. Immunol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1535","DOI":"10.1093\/ps\/85.9.1535","article-title":"Feed Withdrawal Alters Small-Intestinal Morphology and Mucus of Broilers","volume":"85","author":"Thompson","year":"2006","journal-title":"Poult. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Dom\u00ednguez-Negrete, A., G\u00f3mez-Rosales, S., Angeles, M.L., L\u00f3pez-Hern\u00e1ndez, L.H., Reis-de-Souza, T.C., L\u00f3pez-Garc\u00eda, Y., Zavala-Franco, A., and T\u00e9llez-Isaias, G. (2019). Effect of the Addition of Humic Substances as Growth Promoter in Broiler Chickens Under Two Feeding Regimens. Animals, 9.","DOI":"10.3390\/ani9121101"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1080\/00071660802538632","article-title":"Managing gut health through nutrition","volume":"50","author":"Choct","year":"2009","journal-title":"Brit. Poult. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"650","DOI":"10.1093\/ps\/83.4.650","article-title":"Nutritional modulation of immune function in broilers","volume":"83","author":"Kidd","year":"2004","journal-title":"Poult. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Dom\u00ednguez-Negrete, A., G\u00f3mez-Rosales, S., Angeles, M.d.L., L\u00f3pez-Hern\u00e1ndez, L.H., de Souza, T.C.R., Latorre-C\u00e1rdenas, J.D., and T\u00e9llez-Isaias, G. (2021). Addition of Different Levels of Humic Substances Extracted from Worm Compost in Broiler Feeds. Animals, 11.","DOI":"10.3390\/ani11113199"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1590\/1806-9061-2021-1450","article-title":"Growth Performance and Tibia Mineraliza-tion of Broiler Chickens Supplemented with a Liquid Extract of Humic Substances","volume":"24","author":"Angeles","year":"2022","journal-title":"Braz. J. Poult. Sci."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Soto-Hernandez, M., Palma-Tenango, M., and Garcia-Mateos, M. (2017). Phenolic Compounds in Maize Grains and Its Nixtamalized Products. Phenolic Compounds\u2014Natural Sources, Importance and Applications, IntechOpen.","DOI":"10.5772\/67213"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"209","DOI":"10.17533\/udea.rccp.324926","article-title":"Escherichia coli lipopolysaccharide affects intestinal mucin secretion in weaned pigs","volume":"28","author":"Zapata","year":"2015","journal-title":"Rev. Colom. Cienc. Pec."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1495","DOI":"10.1093\/ps\/84.9.1495","article-title":"Hypobaric hipoxia in ascites resistant and susceptible broiler genetic lines influences gut morphology","volume":"84","author":"Tellez","year":"2005","journal-title":"Poult. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"888","DOI":"10.3382\/ps.2011-01661","article-title":"Effect of metabolic efficiency and intestinal morphology on variability in n-3 polyunsaturated fatty acid enrichment of eggs","volume":"91","author":"Nain","year":"2012","journal-title":"Poult. Sci."},{"key":"ref_24","unstructured":"SAS Institute Inc. (1990). SAS User\u2019s Guide: Statistics, Version, SAS Inst Inc.. [64th ed.]."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1007\/s12602-017-9275-9","article-title":"The Effects of Direct-fed Microbial Supplementation, as an Alternative to Antibiotics, on Growth Performance, Intestinal Immune Status, and Epithelial Barrier Gene Expression in Broiler Chickens","volume":"9","author":"Gadde","year":"2017","journal-title":"Probiotics Antimicrob. Prot."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Koltes, D.A., Lester, H.D., and Frost, M. (2017). Effects of bacitracin methylene disalicylate and diet change on gastrointestinal integrity and endotoxin permeability in the duodenum of broiler chicken. BMC Res. Notes, 10.","DOI":"10.1186\/s13104-017-2781-8"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1093\/ps\/85.3.476","article-title":"Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters, and quantitative morphology","volume":"85","author":"Miles","year":"2006","journal-title":"Poult. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"101563","DOI":"10.1016\/j.psj.2021.101563","article-title":"Effect of blending encapsulated essential oils and organic acids as an antibiotic growth promoter alternative on growth performance and intestinal health in broilers with necrotic enteritis","volume":"101","author":"Pham","year":"2022","journal-title":"Poult. Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1079\/WPS20040017","article-title":"Characteristics of the gastrointestinal microbial communities, with special reference to the chicken","volume":"60","author":"Apajalahti","year":"2004","journal-title":"World\u2019s Poult. Sci. J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.3382\/ps\/pey021","article-title":"Gut barrier function: Effects of (antibiotic) growth promoters on key barrier components and associations with growth performance","volume":"97","author":"Broom","year":"2018","journal-title":"Poult Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1093\/ps\/81.2.227","article-title":"The effects of dietary humate supplementation on broiler growth and carcass yield","volume":"81","author":"Kocabagli","year":"2012","journal-title":"Poult. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1111\/j.1439-0396.2008.00886.x","article-title":"Effects of humic substances supplementation provided through drinking water on performance, carcass traits and meat quality of broilers","volume":"94","author":"Ozturk","year":"2010","journal-title":"J. Anim. Physiol. Anim. Nut."},{"key":"ref_33","first-page":"215","article-title":"Addition of a Worm Leachate as Source of Humic Substances in the Drinking Water of Broiler Chickens","volume":"28","author":"Angeles","year":"2015","journal-title":"Asian-Australas. J. Anim. Sci."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Maguey-Gonz\u00e1lez, J.A., G\u00f3mez-Rosales, S., Angeles, M.L., and T\u00e9llez-Isa\u00edas, G. (2022). Use of Humic Substances from Vermicompost in Poultry. the Global Antimicrobial Resistance Epidemic\u2014Innovative Approaches and Cutting-Edge Solutions, IntechOpen.","DOI":"10.5772\/intechopen.102939"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1046\/j.1439-0396.2002.00383.x","article-title":"Performance and ileal histomorphology of rats treated with humic acid preparations","volume":"86","author":"Yasar","year":"2002","journal-title":"J. Anim. Physiol. Anim. Nutr."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"636","DOI":"10.3382\/ps.2013-03362","article-title":"Differences in intestinal mucin dynamics between germ-free and conventionally reared chickens after mannan-oligosaccharide supplementation","volume":"93","author":"Gamage","year":"2014","journal-title":"Poult. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1093\/ps\/82.2.320","article-title":"Pre-and Posthatch Development of Goblet Cells in the Broiler Small Intestine: Effect of Delayed Access to Feed","volume":"82","author":"Uni","year":"2003","journal-title":"Poult. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3577","DOI":"10.3382\/ps\/pey202","article-title":"Ingestion of Paddy Rice Increases Intestinal Mucin Secretion and Goblet Cell Number and Prevents Dextran Sodium Sulfate-Induced Intestinal Barrier Defect in Chickens","volume":"97","author":"Murai","year":"2018","journal-title":"Poult. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1079\/BJN2001368","article-title":"The Effect of Fasting at Different Ages on Growth and Tissue Dynamics in the Small Intestine of the Young Chick","volume":"86","author":"Geyra","year":"2001","journal-title":"Br. J. Nutr."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1080\/00071660120073151","article-title":"Body and Intestinal Growth of Broiler Chicks on a Commercial Starter Diet. 1. Intestinal Weight and Mucosal Development","volume":"42","author":"Iji","year":"2001","journal-title":"Br. Poult. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2173","DOI":"10.3382\/ps\/pev182","article-title":"Effect of Lactulose Supplementation on Growth Performance, Intestinal Histomorphology, Cecal Microbial Population, and Short-Chain Fatty Acid Composition of Broiler Chickens","volume":"94","author":"Calik","year":"2015","journal-title":"Poult. Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"306","DOI":"10.3382\/japr.2014-00937","article-title":"Function of the digestive system","volume":"23","author":"Svihus","year":"2014","journal-title":"J. Appl. Poult. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"546","DOI":"10.3382\/japr\/pfy027","article-title":"Intestinal Passage and Its Relation to Digestive Processes","volume":"28","author":"Svihus","year":"2019","journal-title":"J. Appl. Poult. Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1186\/s40104-021-00565-3","article-title":"Phenolic compounds as natural feed additives in poultry and swine diets: A review","volume":"12","author":"Mahfuz","year":"2021","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2066","DOI":"10.1093\/jas\/skz075","article-title":"Improved growth performance due to hypertrophied intestinal absorptive epithelial cells by heat-killed Lactobacillus sakei HS-1 in broiler chickens","volume":"97","author":"Khonyoung","year":"2019","journal-title":"J. Anim. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Prakatur, I., Miskulin, M., Pavic, M., Marjanovic, K., Blazicevic, V., Miskulin, I., and Domacinovic, M. (2019). Intestinal Morphology in Broiler Chickens Supplemented with Propolis and Bee Pollen. Animals., 9.","DOI":"10.3390\/ani9060301"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"974","DOI":"10.1093\/ps\/85.6.974","article-title":"Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens","volume":"85","author":"Awad","year":"2006","journal-title":"Poult. Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/S1095-6433(02)00121-6","article-title":"Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis var. natto","volume":"133","author":"Samanya","year":"2002","journal-title":"Comp. Biochem. Physiol. A Mol. Integr. Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1093\/ps\/85.3.505","article-title":"E_cacy of supplementation of alpha-amylase-producing bacterial culture on the performance, nutrient use and gut morphology of broiler chickens fed a corn-based diet","volume":"85","author":"Onderci","year":"2006","journal-title":"Poult. Sci."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/2\/212\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:01:33Z","timestamp":1760119293000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/2\/212"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,6]]},"references-count":49,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,1]]}},"alternative-id":["ani13020212"],"URL":"https:\/\/doi.org\/10.3390\/ani13020212","relation":{},"ISSN":["2076-2615"],"issn-type":[{"type":"electronic","value":"2076-2615"}],"subject":[],"published":{"date-parts":[[2023,1,6]]}}}