{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,21]],"date-time":"2026-07-21T19:57:56Z","timestamp":1784663876597,"version":"3.55.0"},"reference-count":46,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2022,5,12]],"date-time":"2022-05-12T00:00:00Z","timestamp":1652313600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"university grant","award":["Foper-2017-00069"],"award-info":[{"award-number":["Foper-2017-00069"]}]},{"name":"university grant","award":["Foper-2018-00212"],"award-info":[{"award-number":["Foper-2018-00212"]}]},{"name":"university grant","award":["#550509"],"award-info":[{"award-number":["#550509"]}]},{"name":"Consejo Nacional de Ciencia y Tecnolog\u00eda (CONACYT)","award":["Foper-2017-00069"],"award-info":[{"award-number":["Foper-2017-00069"]}]},{"name":"Consejo Nacional de Ciencia y Tecnolog\u00eda (CONACYT)","award":["Foper-2018-00212"],"award-info":[{"award-number":["Foper-2018-00212"]}]},{"name":"Consejo Nacional de Ciencia y Tecnolog\u00eda (CONACYT)","award":["#550509"],"award-info":[{"award-number":["#550509"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>This study aimed to investigate the effect of feeding insoluble fiber on the microbiota and metabolites of the caecum and feces of rabbits recovering from epizootic rabbit enteropathy relative to non-infected rabbits. Rabbits that had either recovered from epizootic rabbit enteropathy or ones that had never had epizootic rabbit enteropathy were fed on a diet of 32% or 36% neutral detergent fiber until they were 70 days of age. At this point, the short-chain fatty acid and ammonia levels were measured in caecotroph and fecal samples and compared using 2 \u00d7 2 ANOVA. The microbial composition of the samples was also analyzed using next-generation sequencing and compared by PERMANOVA. Caecotrophic samples from previously affected rabbits on lower fiber diets had higher short-chain fatty acid contents and higher species diversity index values for some indices (p &lt; 0.05), although the fecal samples showed lower species diversity levels (p &lt; 0.05). In addition, the PERMANOVA analyses demonstrated that differences were detected in the microbial composition of both fecal and caecotrophic samples, depending on the disease status at the outset of the experiment (p &lt; 0.05). The results of this work show that, although there is some potential in the use of high-fiber diets for the treatment of rabbits that have had epizootic rabbit enteropathy, they are not able to produce the same digestive tract properties as those seen in rabbits that have never had the condition. This is true even after the rabbits have recovered from epizootic rabbit enteropathy.<\/jats:p>","DOI":"10.3390\/pathogens11050571","type":"journal-article","created":{"date-parts":[[2022,5,12]],"date-time":"2022-05-12T05:10:32Z","timestamp":1652332232000},"page":"571","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Effect of Feeding Insoluble Fiber on the Microbiota and Metabolites of the Caecum and Feces of Rabbits Recovering from Epizootic Rabbit Enteropathy Relative to Non-Infected Rabbits"],"prefix":"10.3390","volume":"11","author":[{"given":"Xiao-Haitzi Daniel","family":"Pu\u00f3n-Pel\u00e1ez","sequence":"first","affiliation":[{"name":"Doctorado en Ciencias Biol\u00f3gicas, Facultad de Ciencias Naturales, Universidad Aut\u00f3noma de Quer\u00e9taro, Avenida de las Ciencias S\/N, Juriquilla, Delegaci\u00f3n Santa Rosa J\u00e1uregui, Quer\u00e9taro C.P. 76230, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3839-9072","authenticated-orcid":false,"given":"Neil Ross","family":"McEwan","sequence":"additional","affiliation":[{"name":"School of Pharmacy & Life Sciences, Robert Gordon University, Garthdee House, Garthdee Rd, Aberdeen AB10 7GJ, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0821-0067","authenticated-orcid":false,"given":"Roberto Carlos","family":"\u00c1lvarez-Mart\u00ednez","sequence":"additional","affiliation":[{"name":"Facultad de Ciencias Naturales, Universidad Aut\u00f3noma de Quer\u00e9taro, Av. Junipero Serra, Antiguo Aeropuerto, Campus Aeropuerto S\/N, Santiago de Quer\u00e9taro, Quer\u00e9taro C.P. 76140, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6684-4765","authenticated-orcid":false,"given":"Gerardo","family":"Mariscal-Land\u00edn","sequence":"additional","affiliation":[{"name":"Centro Nacional de Investigaci\u00f3n en Fisiolog\u00eda Animal INIFAP, Km. 1, Carretera a Col\u00f3n, Col. Ajuchitl\u00e1n Col\u00f3n, Quer\u00e9taro C.P. 76280, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4689-0419","authenticated-orcid":false,"given":"Gerardo Manuel","family":"Nava-Morales","sequence":"additional","affiliation":[{"name":"Facultad de Qu\u00edmica, Universidad Aut\u00f3noma de Quer\u00e9taro, Cerro de las Campanas S\/N, Santiago de Quer\u00e9taro, Quer\u00e9taro C.P. 76010, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8892-6390","authenticated-orcid":false,"given":"Juan","family":"Mosqueda","sequence":"additional","affiliation":[{"name":"Cuerpo Acad\u00e9mico Salud Animal y Microbiolog\u00eda Ambiental, Facultad de Ciencias Naturales, Universidad Aut\u00f3noma de Quer\u00e9taro, Avenida de las Ciencias S\/N, Juriquilla, Delegaci\u00f3n Santa Rosa J\u00e1uregui, Quer\u00e9taro C.P. 76230, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4703-2010","authenticated-orcid":false,"given":"Andrea Margarita","family":"Olvera-Ram\u00edrez","sequence":"additional","affiliation":[{"name":"Cuerpo Acad\u00e9mico Salud Animal y Microbiolog\u00eda Ambiental, Facultad de Ciencias Naturales, Universidad Aut\u00f3noma de Quer\u00e9taro, Avenida de las Ciencias S\/N, Juriquilla, Delegaci\u00f3n Santa Rosa J\u00e1uregui, Quer\u00e9taro C.P. 76230, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,5,12]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/j.livsci.2009.05.010","article-title":"Risk factors for an acute expression of Epizootic Rabbit Enteropathy syndrome in rabbits after weaning in French kindling-to-finish farms","volume":"125","author":"Jobert","year":"2009","journal-title":"Livest. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"B\u00e4uerl, C., Collado, M.C., Z\u00fa\u00f1iga, M., Blas, E., and P\u00e9rez, G. (2014). Changes in Caecal Microbiota and Mucosal Gene Expression Revealed New Aspects of Epizootic Rabbit Enteropathy. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0105707"},{"key":"ref_3","first-page":"167","article-title":"Etiopatogenia de la enteropat\u00eda epizo\u00f3tica del conejo","volume":"139","author":"Rosell","year":"2005","journal-title":"Bolet\u00edn Cunicult. Lagomorpha"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.rvsc.2007.04.018","article-title":"Studies on the evolution, pathology, and immunity of commercial fattening rabbits affected with epizootic outbreaks of diarrhoeas in Mexico: A case report","volume":"84","author":"Cedillo","year":"2008","journal-title":"Res. Veter. Sci."},{"key":"ref_5","first-page":"14","article-title":"Identificaci\u00f3n de infecciones digestivas en conejos: Orientaciones para optimizar la prevencion y el control","volume":"176","author":"Perez","year":"2015","journal-title":"Bolet\u00edn Cunicult. Lagomorpha"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.tvjl.2014.12.036","article-title":"Efficacy and tolerability of early administration of valnemulin hydrochloride premix on epizootic rabbit enteropathy","volume":"204","author":"Dip","year":"2015","journal-title":"Vet. J."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Pu\u00f3n Pel\u00e1ez, X.-H.D., McEwan, N.R., G\u00f3mez-Soto, J.G., \u00c1lvarez-Mart\u00ednez, R.C., and Olvera-Ram\u00edrez, A.M. (2020). Metataxonomic and histopathological study of rabbit epizootic enteropathy in Mexico. Animals, 10.","DOI":"10.3390\/ani10060936"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1093\/jac\/dki273","article-title":"The susceptibility to growth-promoting antibiotics of Enterococcus faecium isolates from pigs and chickens in Europe","volume":"56","author":"Bywater","year":"2005","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1186\/s13567-018-0617-8","article-title":"Gut colonization by a novel Clostridium species is associated with the onset of epizootic rabbit enteropathy","volume":"49","author":"Djukovic","year":"2018","journal-title":"Vet. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1111\/j.1365-2672.2007.03309.x","article-title":"The effect of medicated diets and level of feeding on caecal microbiota of lactating rabbit does","volume":"103","author":"Abecia","year":"2007","journal-title":"J. Appl. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1111\/j.1574-6968.2007.00746.x","article-title":"Effect of antibiotics on the bacterial population of the rabbit caecum","volume":"272","author":"Abecia","year":"2007","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1079\/BJN19840031","article-title":"Absorption and metabolism of the volatile fatty acids in the hind-gut of the rabbit","volume":"51","author":"Marty","year":"1984","journal-title":"Br. J. Nutr."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Zhao, J., Bai, Y., Zhang, G., Liu, L., and Lai, L. (2020). Relationship between Dietary Fibre Fermentation and Volatile Fatty Acids Concentration in Growing Pigs. Animals, 10.","DOI":"10.3390\/ani10020263"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Oczkowicz, M., Szmato\u0142a, T., \u015awi\u0105tkiewicz, M., Pawlina-Tyszko, K., Gurgul, A., and Z\u0105bek, T. (2018). Corn dried distillers grains with solubles (cDDGS) in the diet of pigs change the expression of adipose genes that are potential therapeutic targets in metabolic and cardiovascular diseases. BMC Genom., 19.","DOI":"10.1186\/s12864-018-5265-x"},{"key":"ref_15","unstructured":"RStudio Team (2020). RStudio: Integrated Development for R, RStudio, PBC. Available online: http:\/\/www.rstudio.com\/."},{"key":"ref_16","first-page":"137","article-title":"Epizootic rabbit enteropathy (ERE): A review of current knowledge","volume":"14","author":"McEwan","year":"2018","journal-title":"Eur. Sci. J."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1017\/S1751731113001079","article-title":"Engineering the rabbit digestive ecosystem to improve digestive health and efficacy","volume":"7","author":"Combes","year":"2013","journal-title":"Animal"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1017\/S1751731115001822","article-title":"Effect of purple loosestrife (Lythrum salicaria) diet supplementation in rabbit nutrition on performance, digestibility, health and meat quality","volume":"10","author":"Kovitvadhi","year":"2016","journal-title":"Animal"},{"key":"ref_19","first-page":"9","article-title":"Effects of type and level of fibre on digestive physiology and performance in reproducing and growing rabbits","volume":"15","author":"Alvarez","year":"2007","journal-title":"World Rabbit Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1017\/S1751731116002007","article-title":"Impact of feed restriction and housing hygiene conditions on specific and inflammatory immune response, the caecal bacterial community and the survival of young rabbits","volume":"11","author":"Combes","year":"2017","journal-title":"Animal"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1139\/cjm-2015-0201","article-title":"Impact of dietary fibre\/starch ratio in shaping caecal microbiota in rabbits","volume":"61","author":"Zhu","year":"2015","journal-title":"Can. J. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1111\/j.1365-2672.1985.tb01475.x","article-title":"Nitrogen metabolism by the microbial flora of the rabbit caecum","volume":"58","author":"Forsythe","year":"1985","journal-title":"J. Appl. Bacteriol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1051\/vetres:2005021","article-title":"Epizootic Rabbit Enteropathy: Experimental transmission and clinical characterization","volume":"36","author":"Licois","year":"2005","journal-title":"Vet. Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"261","DOI":"10.4995\/wrs.2017.5230","article-title":"Pyrosequencing study of caecal bacterial community of rabbit does and kits from a farm affected by epizootic rabbit enteropathy","volume":"25","author":"Abecia","year":"2017","journal-title":"World Rabbit Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"177","DOI":"10.4995\/wrs.2011.941","article-title":"Characterization of Clostridium perfringens presence and concentration of its \u03b1-toxin in the caecal contents of fattening rabbits suffering from digestive diseases","volume":"19","author":"Romero","year":"2011","journal-title":"World Rabbit Sci."},{"key":"ref_26","unstructured":"Xiccato, G., Trocino, A., Carraro, L., Fragkiadakis, M., and Majolini, D. (2008, January 10\u201313). Digestible fibre to starch ratio and antibiotic treatment time in growing rabbits affected by epizootic rabbit enteropathy. Proceedings of the 9th World Rabbit Congress, Verona, Italy."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.femsle.2005.01.028","article-title":"Molecular profiling of bacterial species in the rabbit caecum","volume":"244","author":"Abecia","year":"2005","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1111\/j.1574-6941.2008.00611.x","article-title":"Potential core species and satellite species in the bacterial community within the rabbit caecum","volume":"66","author":"Monteils","year":"2008","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Crowley, E.J., Kink, J.M., Wilkinson, T., Worgan, H.J., Huson, K.M., Rose, M.T., and McEwan, N.R. (2017). Comparison of the microbial population in rabbits and guinea pigs by next generation sequencing. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0165779"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.tvjl.2012.08.014","article-title":"Pyrosequencing of epizootic rabbit enteropathy inocula and rabbit caecal samples","volume":"196","author":"Huybens","year":"2013","journal-title":"Vet. J."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1080\/01621459.1992.10475194","article-title":"Estimating the number of classes via sample coverage","volume":"87","author":"Chao","year":"1992","journal-title":"J. Am. Stat. Assoc."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1038\/163688a0","article-title":"Measurement of diversity","volume":"163","author":"Simpson","year":"1949","journal-title":"Nature"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2089","DOI":"10.4014\/jmb.1709.09027","article-title":"Deciphering Diversity Indices for a Better Understanding of Microbial Communities","volume":"27","author":"Kim","year":"2017","journal-title":"J. Microbiol. Biotechnol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"12489","DOI":"10.1038\/s41598-018-30178-2","article-title":"The underlying microbial mechanism of epizootic rabbit enteropathy triggered by a low fibre diet","volume":"8","author":"Jin","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2144","DOI":"10.3389\/fmicb.2018.02144","article-title":"Rabbit Microbiota Changes Throughout the Intestinal Tract","volume":"9","author":"Piles","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_36","first-page":"3623274","article-title":"Zearalenone Changes the Diversity and Composition of Caecum Microbiota in Weaned Rabbit","volume":"8","author":"Li","year":"2018","journal-title":"Biomed. Res. Int."},{"key":"ref_37","unstructured":"Comisi\u00f3n \u00c9tica Asesora Para la Experimentaci\u00f3n Animal (2013). Evaluaci\u00f3n del Dolor en el Conejo, CEA. Available online: http:\/\/cea.unizar.es\/Disenos_experimentales\/Anestesia%20y%20analgesia\/Evaluacion_dolor\/Evaluacion_dolor_en_conejos.pdf."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"De Blas, C., and Wiseman, J. (2010). Nutrition and Feeding Strategy: Interactions with Pathology. Nutrition of the Rabbit, CABI.","DOI":"10.1079\/9781845936693.0000"},{"key":"ref_39","unstructured":"AOAC (1990). Official Methods of Analysis, Association of Official Analytical Chemists. [15th ed.]."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1625","DOI":"10.1093\/ps\/86.8.1625","article-title":"Effects of Dietary Fibre and Reduced Crude Protein on Ammonia Emission from Laying-Hen Manure","volume":"86","author":"Roberts","year":"2007","journal-title":"Poult. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1021\/ac60038a038","article-title":"Kjeldahl Method for Total Nitrogen","volume":"22","author":"Kirk","year":"1950","journal-title":"Anal. Chem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina Sequence Data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_43","unstructured":"Andrews, S. (2020, July 01). A Quality Control Tool for High Throughput Sequence Data. Available online: https:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.12688\/f1000research.8986.1","article-title":"Bioconductor workflow for microbiome data analysis: From raw reads to community analyses","volume":"5","author":"Callahan","year":"2016","journal-title":"F1000Research"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Far\u00edas-Kovac, C., Nicodemus, N., Delgado, R., Ocasio-Vega, C., Noboa, T., Allam-Sayed Abdelrasoul, R., Caraba\u00f1o, R., and Garc\u00eda, J. (2020). Effect of Dietary Insoluble and Soluble Fibre on Growth Performance, Digestibility, and Nitrogen, Energy, and Mineral Retention Efficiency in Growing Rabbits. Animals, 10.","DOI":"10.3390\/ani10081346"},{"key":"ref_46","unstructured":"Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O\u2019Hara, R.B., Simpson, G.L., and Solymos, P. (2020, July 01). Community Ecology Package. Available online: https:\/\/github.com\/vegandevs\/vegan."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/5\/571\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:09:39Z","timestamp":1760137779000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/5\/571"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,12]]},"references-count":46,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["pathogens11050571"],"URL":"https:\/\/doi.org\/10.3390\/pathogens11050571","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,12]]}}}