{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T04:29:48Z","timestamp":1789705788951,"version":"4.0.1"},"reference-count":55,"publisher":"Oxford University Press (OUP)","issue":"8","license":[{"start":{"date-parts":[[2019,5,6]],"date-time":"2019-05-06T00:00:00Z","timestamp":1557100800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"Ministry of Business Innovation & Employment","award":["C10X1305"],"award-info":[{"award-number":["C10X1305"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,7,30]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>ABSTRACT: This study examined the impact of weaning age (4 vs. 6 wk) on rumen morphological and metabolic development in artificially reared lambs. Thirty-two mixed-sex lambs (2 to 5 d old) were randomly allocated to 1 of 2 weaning groups: early weaning (EW; 4 wk) and control (Ctrl; 6 wk). Lambs were individually penned and fed milk replacer (MR; 24% CP and 25% fat, DM basis) at 20% of their corresponding initial BW. Weaning was achieved by gradual reduction of MR allowance over a period of 3 wk using a step-down procedure. Concentrate and meadow hay were offered ad libitum from 1 d of the study until 6 wk, when lambs were transferred to a mixed sward pasture. At week 4, individual DMI were recorded and blood samples collected to measure \u03b2-hydroxybutyrate (BHBA) and NEFA. Eight animals per group were euthanized at week 4 and 16 to evaluate short chain fatty acids (SCFA) and histomorphometry of the rumen walls: dorsal (DS), ventral (VS), dorsal blind (DBS), and ventral blind (VBS) sacs. Linear mixed models were used to analyze the effect of weaning treatments at week 4 and 16, and to compare between timepoints and between rumen sites. Dry matter intake and rumen SCFA profiles were similar between groups (P &gt; 0.10) at week 4 and 16. Plasma concentrations of BHBA were greater (P = 0.03) in EW than in Ctrl lambs, while NEFA did not differ (P &gt; 0.10) between groups at week 4. No effect of weaning age on rumen empty weight, and papillae density, length, width, surface area ratio, and muscle layer thickness at any of the 4 rumen sites was found (P &gt; 0.10) at either week 4 or week 16, except for greater (P = 0.02) papillae epithelium thickness in the DBS at week 4 in EW than Ctrl lambs. Papillae morphology and muscular thickness differed across rumen sites at week 4 and week 16 (P &lt; 0.05), except for papillae density and surface area ratio at 4 week (P &gt; 0.10). Rumen papillae length, width, and muscle layer thickness increased while papillae density and surface area ratio decreased (P &lt; 0.05) between 4 and 16 wk. The results of this study indicate that morphological and physiological development of the rumen can be accelerated to support weaning of artificially reared lambs at 4 wk, using a step-down weaning system. Morphological differences between rumen sacs denote that future studies in lambs evaluating the impact of different diets should involve representative sampling across the rumen rather than a single site to more accurately study rumen development and ontogenic changes.<\/jats:p>","DOI":"10.1093\/jas\/skz148","type":"journal-article","created":{"date-parts":[[2019,5,6]],"date-time":"2019-05-06T13:44:14Z","timestamp":1557150254000},"page":"3498-3510","source":"Crossref","is-referenced-by-count":33,"title":["Impact of weaning age on rumen development in artificially reared lambs1"],"prefix":"10.1093","volume":"97","author":[{"given":"Omar Cristobal","family":"Carballo","sequence":"first","affiliation":[{"name":"Animal Nutrition & Physiology Team, AgResearch Limited, Palmerston North, New Zealand"},{"name":"School of Veterinary Sciences, Massey University, Palmerston North, New Zealand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muhammad Ajmal","family":"Khan","sequence":"additional","affiliation":[{"name":"Animal Nutrition & Physiology Team, AgResearch Limited, Palmerston North, New Zealand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frederik Willem","family":"Knol","sequence":"additional","affiliation":[{"name":"Animal Nutrition & Physiology Team, AgResearch Limited, Palmerston North, New Zealand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah Jeanne","family":"Lewis","sequence":"additional","affiliation":[{"name":"Animal Nutrition & Physiology Team, AgResearch Limited, Palmerston North, New Zealand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David Robert","family":"Stevens","sequence":"additional","affiliation":[{"name":"Farm Systems Team, AgResearch Limited, Mosgiel, New Zealand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard Anthony","family":"Laven","sequence":"additional","affiliation":[{"name":"School of Veterinary Sciences, Massey University, Palmerston North, New Zealand"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Susan Anne","family":"McCoard","sequence":"additional","affiliation":[{"name":"Animal Nutrition & Physiology Team, AgResearch Limited, Palmerston North, New Zealand"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,5,6]]},"reference":[{"key":"2019073016502242900_CIT0001","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/j.rvsc.2011.03.010","article-title":"Rumen fermentation and histology in light lambs as affected by forage supply and lactation length","volume":"92","author":"\u00c1lvarez-Rodr\u00edguez","year":"2012","journal-title":"Res. Vet. Sci"},{"key":"2019073016502242900_CIT0002","volume-title":"Official methods of analysis","author":"AOAC","year":"1990","edition":"15"},{"key":"2019073016502242900_CIT0003","volume-title":"Official methods of analysis","author":"AOAC","year":"2010","edition":"18"},{"key":"2019073016502242900_CIT0004","volume-title":"Official methods of analysis","author":"AOAC","year":"2012","edition":"19"},{"key":"2019073016502242900_CIT0005","doi-asserted-by":"crossref","first-page":"1796","DOI":"10.1128\/AEM.64.5.1796-1804.1998","article-title":"Ammonia-hyperproducing bacteria from New Zealand ruminants","volume":"64","author":"Attwood","year":"1998","journal-title":"Appl. Environ. Microbiol"},{"key":"2019073016502242900_CIT0006","doi-asserted-by":"crossref","first-page":"E55","DOI":"10.3168\/jds.S0022-0302(04)70061-2","article-title":"Rumen development, intestinal growth and hepatic metabolism in the pre- and postweaning ruminant","volume":"87","author":"Baldwin","year":"2004","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0007","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/j.smallrumres.2004.12.008","article-title":"Evaluation of lamb performance and costs in motherless rearing of German Grey Heath sheep under field conditions using automatic feeding systems","volume":"60","author":"Bimczok","year":"2005","journal-title":"Small Rumin. Res"},{"key":"2019073016502242900_CIT0090","article-title":"Castells, L., A. Bach, G. Araujo, C. Montoro, and M. Terr\u00e9. 2012. Effect of different forage sources on performance and feeding behavior of Holstein calves. J. Dairy Sci. 95(1):286\u2013293. doi:10.3168\/jds.2011-4405"},{"key":"2019073016502242900_CIT0008","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1002\/jmor.10729","article-title":"The intraruminal papillation gradient in wild ruminants of different feeding types: Implications for rumen physiology","volume":"270","author":"Clauss","year":"2009","journal-title":"J. Morphol"},{"key":"2019073016502242900_CIT0009","unstructured":"Corson D. , G.Waghorn, M.Ulyatt, and J.Lee. 1999. NIRS: Forage analysis and livestock feeding. In: Proc. of the New Zealand Grassland Association. 1999. Vol. 61. Hawkes Bay, NZ. p. 127\u2013132."},{"key":"2019073016502242900_CIT0010","doi-asserted-by":"publisher","first-page":"7624","DOI":"10.3168\/jds.2016-11097","article-title":"Validation of a calf-side \u03b2-hydroxybutyrate test and its utility for estimation of starter intake in dairy calves around weaning","volume":"99","author":"Deelen","year":"2016","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0011","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1079\/BJN19730114","article-title":"Changes in some physical characteristics of the digesta in the reticulo-rumen of cows fed once daily","volume":"29","author":"Evans","year":"1973","journal-title":"Br. J. Nutr"},{"key":"2019073016502242900_CIT0012","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1111\/j.1469-7998.1999.tb00761.x","article-title":"Seasonal changes in the rumen morphology of Himalayan tahr (Hemitragus jemlahicus) in the Two Thumb Range, South Island, New Zealand","volume":"249","author":"Forsyth","year":"1999","journal-title":"J. Zool"},{"key":"2019073016502242900_CIT0013","article-title":"Comparative microbiology of the alimentary tract","author":"Giesecke","year":"1970","journal-title":"In: Phillipson A.T., editor, Physiology of digestion and metabolism in the ruminant, oriel press, Newcastle upon Tyne (1970), pp. 306\u2013318."},{"key":"2019073016502242900_CIT0014","doi-asserted-by":"publisher","first-page":"2534","DOI":"10.3168\/jds.S0022-0302(97)76207-6","article-title":"A new method of measuring diet abrasion and its effect on the development of the forestomach","volume":"80","author":"Greenwood","year":"1997","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0015","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1071\/an15526","article-title":"Dose-response effect of nitrate on hydrogen distribution between rumen fermentation end products: An in vitro approach","volume":"56","author":"Guyader","year":"2016","journal-title":"Anim. Prod. Sci"},{"key":"2019073016502242900_CIT0016","doi-asserted-by":"publisher","first-page":"667","DOI":"10.4141\/cjas84-075","article-title":"Postweaning performance of artificially reared lambs weaned at 21 vs. 28 days of age under two postweaning housing regimens","volume":"64","author":"Heaney","year":"1984","journal-title":"Can. J. Anim. Sci"},{"key":"2019073016502242900_CIT0017","doi-asserted-by":"publisher","first-page":"324","DOI":"10.3168\/jds.S0022-0302(05)72691-6","article-title":"Technical note: Technique for dissection and analysis of the rumen in young calves","volume":"88","author":"Hill","year":"2005","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0091","article-title":"Jasper, J., and D. M. Weary. 2002. Effects of ad libitum milk intake on dairy calves. J. Dairy Sci. 85(11):3054\u20133058. doi:10.3168\/jds.S0022-0302(02)74391-9"},{"key":"2019073016502242900_CIT0018","first-page":"391","article-title":"Energy metabolism in the developing rumen epithelium","volume":"Vol. 3.","author":"Jesse","year":"2005","journal-title":"In: Biology of Growing Animals"},{"key":"2019073016502242900_CIT0019","doi-asserted-by":"publisher","first-page":"3464","DOI":"10.2527\/jas.2015-9912","article-title":"Methane emissions changed nonlinearly with graded substitution of alfalfa silage with corn silage and corn grain in the diet of sheep and relation with rumen fermentation characteristics in vivo and in vitro","volume":"94","author":"Jonker","year":"2016","journal-title":"J. Anim. Sci"},{"key":"2019073016502242900_CIT0020","unstructured":"Jonker A. , G.Molano, E.Sandoval, P.Taylor, C.Antwi, and G.Cosgrove. 2014. BRIEF COMMUNICATION: Methane emissions by sheep offered high sugar or conventional perennial ryegrass at two allowances. In: Proc. of the New Zealand Society of Animal Production. 2014. Vol. 74. Naiper, NZ p. 145\u2013147."},{"key":"2019073016502242900_CIT0021","doi-asserted-by":"publisher","first-page":"953","DOI":"10.1152\/ajplegacy.1969.216.4.953","article-title":"Hepatic and portal metabolism of glucose, free fatty acids, and ketone bodies in the sheep","volume":"216","author":"Katz","year":"1969","journal-title":"Am. J. Physiol"},{"key":"2019073016502242900_CIT0022","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.livsci.2016.02.007","article-title":"Rumen papillae morphology of beef steers relative to gain and feed intake and the association of volatile fatty acids with kallikrein gene expression","volume":"187","author":"Kern","year":"2016","journal-title":"Livest. Sci"},{"key":"2019073016502242900_CIT0023","doi-asserted-by":"crossref","first-page":"885","DOI":"10.3168\/jds.2015-9975","article-title":"Invited review: Transitioning from milk to solid feed in dairy heifers","volume":"99","author":"Khan","year":"2016","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0024","doi-asserted-by":"publisher","first-page":"3376","DOI":"10.3168\/jds.2007-0104","article-title":"Structural growth, rumen development, and metabolic and immune responses of Holstein male calves fed milk through step-down and conventional methods","volume":"90","author":"Khan","year":"2007","journal-title":"J Dairy Sci"},{"key":"2019073016502242900_CIT0025","doi-asserted-by":"publisher","first-page":"876","DOI":"10.3168\/jds.S0022-0302(07)71571-0","article-title":"Pre- and postweaning performance of holstein female calves fed milk through step-down and conventional methods","volume":"90","author":"Khan","year":"2007","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0026","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.3168\/jds.2010-3733","article-title":"Invited review: Effects of milk ration on solid feed intake, weaning, and performance in dairy heifers","volume":"94","author":"Khan","year":"2011","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0027","doi-asserted-by":"publisher","first-page":"1990","DOI":"10.2527\/2000.7871990x","article-title":"Sheep rumen metabolic development in response to age and dietary treatments","volume":"78","author":"Lane","year":"2000","journal-title":"J. Anim. Sci"},{"key":"2019073016502242900_CIT0028","doi-asserted-by":"crossref","first-page":"1538","DOI":"10.2527\/2002.8061538x","article-title":"Developmental changes in ketogenic enzyme gene expression during sheep rumen development","volume":"80","author":"Lane","year":"2002","journal-title":"J. Anim. Sci"},{"key":"2019073016502242900_CIT0029","doi-asserted-by":"publisher","first-page":"740","DOI":"10.3168\/jds.S0022-0302(97)75993-9","article-title":"Effect of volatile fatty acid infusion on development of the rumen epithelium in neonatal sheep","volume":"80","author":"Lane","year":"1997","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0030","doi-asserted-by":"publisher","first-page":"1336","DOI":"10.3168\/jds.S0022-0302(04)73283-X","article-title":"Development and analysis of a rumen tissue sampling procedure","volume":"87","author":"Lesmeister","year":"2004","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0031","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.anifeedsci.2016.04.006","article-title":"Effects of lamb early starter feeding on the expression of genes involved in volatile fatty acid transport and pH regulation in rumen tissue","volume":"217","author":"Liu","year":"2016","journal-title":"Anim. Feed Sci. Technol"},{"key":"2019073016502242900_CIT0092","article-title":"Luo, D., S. Ganesh, and J. Koolaard. 2018. Calculate predicted means for linear models. https:\/\/CRAN.R-project.org\/package=predictmeans"},{"key":"2019073016502242900_CIT0032","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1111\/j.1469-7998.2000.tb00598.x","article-title":"Diet composition, rumen papillation and maintenance of carcass mass in female Norwegian reindeer (Rangifer tarandus tarandus) in winter","volume":"251","author":"Mathiesen","year":"2000","journal-title":"J. Zool"},{"key":"2019073016502242900_CIT0033","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1007\/s10142-013-0351-2","article-title":"Ruminal epithelium transcriptome dynamics in response to plane of nutrition and age in young holstein calves","volume":"14","author":"Naeem","year":"2014","journal-title":"Funct. Integr. Genomics"},{"key":"2019073016502242900_CIT0034","doi-asserted-by":"publisher","first-page":"1807","DOI":"10.3168\/jds.2011-4709","article-title":"Role of metabolic and cellular proliferation genes in ruminal development in response to enhanced plane of nutrition in neonatal Holstein calves1","volume":"95","author":"Naeem","year":"2012","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0035","doi-asserted-by":"publisher","first-page":"1169","DOI":"10.1007\/s11250-011-9819-z","article-title":"Rumen development and growth of Balouchi lambs offered alfalfa hay pre- and post-weaning","volume":"43","author":"Norouzian","year":"2011","journal-title":"Trop. Anim. Health Prod"},{"key":"2019073016502242900_CIT0036","first-page":"1","article-title":"The effects of varying the quantity and distribution of liquid feed in lambs reared artificially","volume":"11","author":"Owen","year":"1969","journal-title":"Anim. Prod"},{"key":"2019073016502242900_CIT0037"},{"key":"2019073016502242900_CIT0038","first-page":"119","article-title":"The sheep dairy industry in New Zealand: A review","volume-title":"Proc. of the New Zealand Society of Animal Production. 2015. Vol 75. Dunedin, NZ","author":"Peterson","year":"2015"},{"key":"2019073016502242900_CIT0039","volume-title":"nlme: Linear and nonlinear mixed efects models. R package","author":"Pinheiro","year":"2018"},{"key":"2019073016502242900_CIT0040","doi-asserted-by":"publisher","first-page":"250","DOI":"10.3168\/jds.S0022-0302(91)78167-8","article-title":"Changes in blood glucose, nonesterified fatty acids, and ketones in response to weaning and feed intake in young calves","volume":"74","author":"Quigley","year":"1991","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0041","volume-title":"R: A language and environment for statistical computing","author":"R CoreTeam","year":"2016"},{"key":"2019073016502242900_CIT0042","doi-asserted-by":"publisher","first-page":"1109","DOI":"10.3168\/jds.S0022-0302(78)83694-7","article-title":"Rumen epithelial cell proliferation accelerated by rapid increase in intraruminal butyrate","volume":"61","author":"Sakata","year":"1978","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0043","doi-asserted-by":"crossref","first-page":"123","DOI":"10.4141\/cjas2011-095","article-title":"An increase in dietary non-structural carbohydrates alters the structure and metabolism of the rumen epithelium in lambs","volume":"92","author":"Steele","year":"2012","journal-title":"Can. J. Anim. Sci"},{"key":"2019073016502242900_CIT0044","article-title":"The emerging dairy sheep industry in New Zealand","volume-title":"R. Baumont, P. Carr\u00e8re, M. Jouven, G. Lombardi, A. L\u00f3pez-Francos, B. Martin, A. Peeters, and C. Porqueddu editors, Forage resources and ecosystems services provided by Mountain and Mediterranean grassland and rangelands. 2014. CIHEAM\/INRA\/FAO\/ VetAgro Sup Clermont-Ferrand \/ Montpellier SupAgro. Zaragoza, Spain. p 109:741\u2013744.","author":"Stevens","year":"2014"},{"issue":"Part 1","key":"2019073016502242900_CIT0045","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/j.anifeedsci.2005.04.037","article-title":"Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis","volume":"123\u2013124","author":"Tavendale","year":"2005","journal-title":"Anim. Feed Sci. Technol"},{"key":"2019073016502242900_CIT0046","doi-asserted-by":"publisher","first-page":"5217","DOI":"10.3168\/jds.2012-6304","article-title":"What do preweaned and weaned calves need in the diet: A high fiber content or a forage source?","volume":"96","author":"Terr\u00e9","year":"2013","journal-title":"J. Dairy Sci"},{"key":"2019073016502242900_CIT0047","unstructured":"Thompson B. , G.Hofstra, K.Hammond, C.Mackintosh, S.Hoskin, R.Littlejohn, and D.Stevens. 2008. Brief communication: Reticulo-rumen growth and papillae development in farmed red deer calves from four to twelve weeks of age. In: Proceedings of the New Zealand Society of Animal Production. 2008. Vol 68. Brisbane, Australia. p 47\u201348."},{"key":"2019073016502242900_CIT0048","doi-asserted-by":"crossref","DOI":"10.7591\/9781501732355","volume-title":"Nutritional ecology of the ruminant","author":"Van Soest","year":"1994"},{"key":"2019073016502242900_CIT0049","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1021\/jf60067a003","article-title":"Ruminant nutrition: Dietary factors influencing the development of the ruminant stomach","volume":"4","author":"Warner","year":"1956","journal-title":"J. Agric. Food Chem"},{"key":"2019073016502242900_CIT0050","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1071\/AR9680419","article-title":"The digestion of pasture plants by sheep. I. Ruminal production of volatile fatty acids by sheep offered diets of ryegrass and forage oats","volume":"19","author":"Weston","year":"1968","journal-title":"Crop Pasture Sci"},{"key":"2019073016502242900_CIT0051","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1080\/17450399309386097","article-title":"The effect of diet composition on the development of rumen digestion in lambs","volume":"45","author":"Zitnan","year":"1993","journal-title":"Arch. Tierernahr"},{"key":"2019073016502242900_CIT0052","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1080\/17450399809381926","article-title":"Influence of dietary concentrate to forage ratio on the development of rumen mucosa in calves","volume":"51","author":"Zitnan","year":"1998","journal-title":"Arch. Tierernahr"}],"container-title":["Journal of Animal Science"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/jas\/advance-article-pdf\/doi\/10.1093\/jas\/skz148\/28794314\/skz148.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/jas\/article-pdf\/97\/8\/3498\/29020227\/skz148.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,12,10]],"date-time":"2020-12-10T09:57:28Z","timestamp":1607594248000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jas\/article\/97\/8\/3498\/5485923"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,5,6]]},"references-count":55,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2019,5,6]]},"published-print":{"date-parts":[[2019,7,30]]}},"URL":"https:\/\/doi.org\/10.1093\/jas\/skz148","relation":{},"ISSN":["0021-8812","1525-3163"],"issn-type":[{"value":"0021-8812","type":"print"},{"value":"1525-3163","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,8]]},"published":{"date-parts":[[2019,5,6]]}}}