{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,9]],"date-time":"2025-12-09T11:38:45Z","timestamp":1765280325268,"version":"build-2065373602"},"reference-count":51,"publisher":"MDPI AG","issue":"23","license":[{"start":{"date-parts":[[2022,12,2]],"date-time":"2022-12-02T00:00:00Z","timestamp":1669939200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>A total of 168 weaned piglets (average initial body weight of 7.70 \u00b1 0.75 kg) were used in a 4-week feeding trial to investigate the effects of dietary supplementation with protein-chelated zinc (Zn-Pro) alone or combined with a mannan-rich fraction (MRF) to replace high-dose zinc oxide (ZnO) for weaned piglets. The dietary treatments included a basal diet as control (CON), a ZnO diet (basal diet + 1600 mg Zn\/kg from ZnO), a Zn-Pro diet (basal diet + 60 mg Zn\/kg from Zn-Pro), and a MRF plus Zn-Pro diet (MRP, basal diet + 800 mg\/kg MRF + 60 mg Zn\/kg from Zn-Pro). The average daily gain of piglets in the MRP group was higher (p \u2264 0.05) than that in CON and Zn-Pro groups during d 15\u201328 and d 1\u201328 of experiment. The apparent total tract digestibility of dry matter, organic matter, and crude protein in the MRP group was higher (p \u2264 0.05) than that in the CON group. The serum insulin-like growth factor-1 level in the MRP group was markedly higher (p \u2264 0.05) than that of piglets in the other three treatment groups. Piglets fed the Zn-Pro and ZnO diets had greater (p \u2264 0.05) acetic acid in cecal digesta than those fed the CON diet, while the MRP diet had higher (p \u2264 0.05) cecal propionate concentration than those that were fed the CON diet on d 28 of experiment. Moreover, the villus height of ileum in the MRP group tended to be greater than the CON group (p = 0.09). Compared with the CON and MRP groups, the relative abundance of Lactobacillaceae (p = 0.08) and Lachnospiraceae (p = 0.09) in the Zn-Pro group showed an increasing trend. The relative abundance of Prevotellaceae in the Zn-Pro group was significantly lower (p \u2264 0.05) than that in the MRP group. In conclusion, the combined addition of MRF and Zn-Pro acted as a suitable alternative to ZnO to beneficially support the growth performance and intestinal health of weaned piglets, as well as contribute to a lower diarrhea rate and environmental pollution from fecal zinc excretion.<\/jats:p>","DOI":"10.3390\/ani12233407","type":"journal-article","created":{"date-parts":[[2022,12,5]],"date-time":"2022-12-05T04:10:02Z","timestamp":1670213402000},"page":"3407","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Effects of Protein-Chelated Zinc Combined with Mannan-Rich Fraction to Replace High-Dose Zinc Oxide on Growth Performance, Nutrient Digestibility, and Intestinal Health in Weaned Piglets"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8732-9279","authenticated-orcid":false,"given":"Gang","family":"Zhang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China"},{"name":"Nutrition Laboratory of Wellhope Foods Co., Ltd., Shengyang 110164, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jinbiao","family":"Zhao","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4106-3107","authenticated-orcid":false,"given":"Gang","family":"Lin","sequence":"additional","affiliation":[{"name":"Key Laboratory of Agrifood Safety and Quality, Institute of Quality Standards and Testing Technology for Agricultural Products, Chinese Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Beijing 100081, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuhan","family":"Guo","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Defa","family":"Li","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2105-8629","authenticated-orcid":false,"given":"Yi","family":"Wu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3191","DOI":"10.2527\/1999.77123191x","article-title":"Effect of segregated early weaning on postweaning small intestinal development in pigs","volume":"77","author":"Tang","year":"1999","journal-title":"J. Anim. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1186\/2049-1891-4-19","article-title":"The biological stress of early weaned piglets","volume":"4","author":"Campbell","year":"2013","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.anifeedsci.2017.03.001","article-title":"Dietary zinc oxide nanoparticles as growth promoter for weanling pigs","volume":"227","author":"Milani","year":"2017","journal-title":"Anim. Feed Sci. Technol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"187","DOI":"10.5187\/jast.2022.e1","article-title":"Novel zinc sources as antimicrobial growth promoters for monogastric animals: A review","volume":"64","author":"Lei","year":"2022","journal-title":"J. Anim. Sci. Technol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1186\/s13099-015-0071-3","article-title":"High dietary zinc supplementation increases the occurrence of tetracycline and sulfonamide resistance genes in the intestine of weaned pigs","volume":"7","author":"Vahjen","year":"2015","journal-title":"Gut. Pathog."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"264","DOI":"10.5713\/ajas.18.0914","article-title":"Moderate tetrabasic zinc chloride supplementation improves growth performance and reduces diarrhea incidence in weaned pigs","volume":"33","author":"Zhang","year":"2019","journal-title":"Asian Austral. J. Anim. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"162","DOI":"10.15232\/S1080-7446(15)31506-0","article-title":"Effects of pharmacological levels of zinc as zinc oxide on fecal zinc and mineral excretion in weanling pigs","volume":"18","author":"Meyer","year":"2002","journal-title":"Prof. Anim. Sci."},{"key":"ref_8","unstructured":"Ministry of Agriculture of the People\u2019s Republic of China (2017). Announcement of the Ministry of Agriculture of the People\u2019s Republic of China."},{"key":"ref_9","unstructured":"European Medicines Agency (2016, January 17\u201319). European Medicines Agency-News and Events. Proceedings of the Committee for Medicinal Products for Veterinary Use (CVMP) Meeting, London, UK."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Oh, H.J., Kim, M.H., Song, M.H., Lee, J.H., Kim, Y.J., Chang, S.Y., An, J.W., Go, Y.B., Song, D.C., and Cho, H.A. (2021). Effects of replacing medical zinc oxide with different ratios of inorganic: Organic zinc or reducing crude protein diet with mixed feed additives in weaned piglet diets. Animals, 11.","DOI":"10.3390\/ani11113132"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1591","DOI":"10.1017\/S1751731118003361","article-title":"Dietary supplementation of weaned piglets with a yeast-derived mannan-rich fraction modulates cecal microbial profiles, jejunal morphology and gene expression","volume":"13","author":"Fouhse","year":"2019","journal-title":"Animal"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"115111","DOI":"10.1016\/j.anifeedsci.2021.115111","article-title":"Yeast-derived mannan-rich fraction as an alternative for zinc oxide to alleviate diarrhea incidence and improve growth performance in weaned pigs","volume":"281","author":"Zhang","year":"2021","journal-title":"Anim. Feed Sci. Technol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/jan.2015.6","article-title":"A review of 733 published trials on Bio-Mos\u00ae, a mannan oligosaccharide, and Actigen\u00ae, a second generation mannose rich fraction, on farm and companion animals","volume":"3","author":"Spring","year":"2015","journal-title":"J. Appl. Anim. Nutr."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"581","DOI":"10.2527\/2004.822581x","article-title":"Effect of phosphorylated mannans and pharmacological additions of zinc oxide on growth and immunocompetence of weanling pigs","volume":"82","author":"Davis","year":"2004","journal-title":"J. Anim. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1917","DOI":"10.2527\/2002.8071917x","article-title":"Effect of feeding organic and inorganic sources of additional zinc on growth performance and zinc balance in nursery pigs","volume":"80","author":"Case","year":"2002","journal-title":"J. Anim. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.anifeedsci.2014.08.004","article-title":"Mannose rich fraction of Saccharomyces cerevisiae promotes growth and enhances carcass yield in commercially housed grower-finisher pigs","volume":"197","author":"Edwards","year":"2014","journal-title":"Anim. Feed Sci. Technol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Oh, H.-J., Park, Y.-J., Cho, J.H., Song, M.-H., Gu, B.-H., Yun, W., Lee, J.-H., An, J.-S., Kim, Y.-J., and Lee, J.-S. (2021). Changes in diarrhea score, nutrient digestibility, zinc utilization, intestinal immune profiles, and fecal microbiome in weaned piglets by different forms of zinc. Animals, 11.","DOI":"10.3390\/ani11051356"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1093\/jn\/nxz102","article-title":"Grape seed proanthocyanidin affects lipid metabolism via changing gut microflora and enhancing propionate production in weaned pigs","volume":"149","author":"Wu","year":"2019","journal-title":"J. Nutr."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3583","DOI":"10.3168\/jds.S0022-0302(91)78551-2","article-title":"Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition","volume":"74","author":"Robertson","year":"1991","journal-title":"J. Dairy Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"399","DOI":"10.2527\/jas.2015-9767","article-title":"Invited review: Aspects of gastrointestinal tract growth and maturation in the pre- and postweaning period of pigs","volume":"94","author":"Pluske","year":"2016","journal-title":"J. Anim. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1638","DOI":"10.1017\/S1751731120000154","article-title":"Effects of alternative feed additives to medicinal zinc oxide on productivity, diarrhoea incidence and gut development in weaned piglets","volume":"14","author":"Satessa","year":"2020","journal-title":"Animal"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1016\/j.jnutbio.2008.07.007","article-title":"Dietary supplementation with zinc oxide stimulates ghrelin secretion from the stomach of young pigs","volume":"20","author":"Yin","year":"2009","journal-title":"J. Nutr. Biochem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"skac094","DOI":"10.1093\/jas\/skac094","article-title":"Growth performance, immune status, gastrointestinal tract ecology, and function in nursery pigs fed enzymatically treated yeast without or with pharmacological levels of zinc","volume":"100","author":"Christensen","year":"2022","journal-title":"J. Anim. Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"261","DOI":"10.3390\/ani2020261","article-title":"Mannan oligosaccharides in nursery pig nutrition and their potential mode of action","volume":"2","author":"Halas","year":"2012","journal-title":"Animals"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"94","DOI":"10.2527\/jas.2005-686","article-title":"Use of mannan-oligosaccharides and zinc chelate as growth promoters and diarrhea preventative in weaning pigs: Effects on microbiota and gut function","volume":"86","author":"Castillo","year":"2008","journal-title":"J. Anim. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Long, S., He, T., Kim, S.W., Shang, Q., Kiros, T., Mahfuz, S.U., Wang, C., and Piao, X. (2021). Live yeast or live yeast combined with zinc oxide enhanced growth performance, antioxidative capacity, immunoglobulins and gut health in nursery pigs. Animals, 11.","DOI":"10.3390\/ani11061626"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.anifeedsci.2018.06.011","article-title":"Low dose of coated zinc oxide is as effective as pharmacological zinc oxide in promoting growth performance, reducing fecal scores, and improving nutrient digestibility and intestinal morphology in weaned pigs","volume":"245","author":"Lei","year":"2018","journal-title":"Anim. Feed Sci. Technol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"905242","DOI":"10.3389\/fvets.2022.905242","article-title":"Effects of tetrabasic zinc chloride on growth performance, nutrient digestibility and fecal microbial community in weaned piglets","volume":"9","author":"Zhang","year":"2022","journal-title":"Front. Vet. Sci."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Hansen, S.V., N\u00f8rskov, N.P., N\u00f8rgaard, J.V., Woyengo, T.A., Poulsen, H.D., and Nielsen, T.S. (2022). Determination of the optimal level of dietary zinc for newly weaned pigs: A dose-response study. Animals, 12.","DOI":"10.3390\/ani12121552"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1359","DOI":"10.2527\/2004.8251359x","article-title":"Evaluation of various inclusion rates of organic zinc either as polysaccharide or proteinate complex on the growth performance, plasma, and excretion of nursery pigs","volume":"82","author":"Carlson","year":"2004","journal-title":"J. Anim. Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2380","DOI":"10.2527\/2005.83102380x","article-title":"Comparison of growth performance and zinc absorption, retention, and excretion in weanling pigs fed diets supplemented with zinc-polysaccharide or zinc oxide1","volume":"83","author":"Buff","year":"2005","journal-title":"J. Anim. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Bonetti, A., Tugnoli, B., Piva, A., and Grilli, E. (2021). Towards zero zinc oxide: Feeding strategies to manage post-weaning diarrhea in piglets. Animals, 11.","DOI":"10.3390\/ani11030642"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4548","DOI":"10.1093\/jas\/skz318","article-title":"Mannan oligosaccharide supplementation in diets of sow and (or) their offspring improved immunity and regulated intestinal bacteria in piglet","volume":"97","author":"Duan","year":"2019","journal-title":"J. Anim. Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1772","DOI":"10.1093\/jas\/skz065","article-title":"Use of coated nano zinc oxide as an additive to improve the zinc excretion and intestinal morphology of growing pigs","volume":"97","author":"Bai","year":"2019","journal-title":"J. Anim. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Agazzi, A., Perricone, V., Omodei Zorini, F., Sandrini, S., Mariani, E., Jiang, X.R., Ferrari, A., Crestani, M., Nguyen, T.X., and Bontempo, V. (2020). Dietary mannan oligosaccharides modulate gut inflammatory response and improve duodenal villi height in post-weaning piglets improving feed efficiency. Animals, 10.","DOI":"10.3390\/ani10081283"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1017\/S0007114520004948","article-title":"Manno-oligosaccharide attenuates inflammation and intestinal epithelium injury in weaned pigs upon enterotoxigenic Escherichia coli K88 challenge","volume":"126","author":"Yu","year":"2021","journal-title":"Br. J. Nutr."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1111\/j.1439-0396.2004.00488.x","article-title":"Additional dietary zinc for weaning piglets is associated with elevated concentrations of serum IGF-I","volume":"88","author":"Carlson","year":"2004","journal-title":"J. Anim. Physiol. Anim. Nutr."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.5713\/ajas.2008.80057","article-title":"The growth-promoting effect of tetrabasic zinc chloride is associated with elevated concentration of growth hormone and ghrelin","volume":"21","author":"Zhang","year":"2008","journal-title":"Asian Austral. J. Anim. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/S0739-7240(00)00081-3","article-title":"Effects of weaning on somatotrophic gene expression and circulating levels of insulin-like growth factor-1 (IGF-1) and IGF-2 in pigs","volume":"19","author":"Matteri","year":"2000","journal-title":"Domest. Anim. Endocrinol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1379","DOI":"10.1111\/asj.12579","article-title":"Nanosize of zinc oxide and the effects on zinc digestibility, growth performances, immune response and serum parameters of weanling piglets","volume":"87","author":"Li","year":"2016","journal-title":"Anim. Sci. J."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"84","DOI":"10.3389\/fcimb.2015.00084","article-title":"Insights into the role of Erysipelotrichaceae in the human host","volume":"5","author":"Kaakoush","year":"2015","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"114312","DOI":"10.1016\/j.anifeedsci.2019.114312","article-title":"Effects of nano zinc oxide as an alternative to pharmacological dose of zinc oxide on growth performance, diarrhea, immune responses, and intestinal microflora profile in weaned piglets","volume":"258","author":"Sun","year":"2019","journal-title":"Anim. Feed Sci. Technol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1111\/1574-6941.12233","article-title":"The impact of high dietary zinc oxide on the development of the intestinal microbiota in weaned piglets","volume":"87","author":"Starke","year":"2014","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"825","DOI":"10.3389\/fmicb.2017.00825","article-title":"Dietary high zinc oxide modulates the microbiome of ileum and colon in weaned piglets","volume":"8","author":"Yu","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1186\/s40104-021-00573-3","article-title":"Impact of sugar beet pulp and wheat bran on serum biochemical profile, inflammatory responses and gut microbiota in sows during late gestation and lactation","volume":"12","author":"Shang","year":"2021","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"64878","DOI":"10.18632\/oncotarget.17612","article-title":"Dietary ZnO nanoparticles alters intestinal microbiota and inflammation response in weaned piglets","volume":"8","author":"Xia","year":"2017","journal-title":"Oncotarget"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e00209-19","DOI":"10.1128\/mSystems.00209-19","article-title":"A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans","volume":"4","author":"Brahe","year":"2019","journal-title":"mSystems"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"5999","DOI":"10.1007\/s00253-020-10665-1","article-title":"Lizhong decoction ameliorates ulcerative colitis in mice via modulating gut microbiota and its metabolites","volume":"104","author":"Zou","year":"2020","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.aninu.2021.09.012","article-title":"The interaction among gut microbes, the intestinal barrier and short chain fatty acids","volume":"9","author":"Ma","year":"2021","journal-title":"Anim. Nutr."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Zhang, Y., Chen, H., Zhu, W., and Yu, K.F. (2019). Cecal infusion of sodium propionate promotes intestinal development and jejunal barrier function in growing pigs. Animals, 9.","DOI":"10.3390\/ani9060284"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1084","DOI":"10.5713\/ajas.2007.1084","article-title":"Effects of different dietary levels of mannanoligosaccharide on growth performance and gut development of broiler chickens","volume":"20","author":"Yang","year":"2007","journal-title":"Asian Austral. J. Anim. Sci."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/12\/23\/3407\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:33:16Z","timestamp":1760146396000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/12\/23\/3407"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,2]]},"references-count":51,"journal-issue":{"issue":"23","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["ani12233407"],"URL":"https:\/\/doi.org\/10.3390\/ani12233407","relation":{},"ISSN":["2076-2615"],"issn-type":[{"type":"electronic","value":"2076-2615"}],"subject":[],"published":{"date-parts":[[2022,12,2]]}}}