{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T14:44:43Z","timestamp":1790952283106,"version":"4.1.0"},"reference-count":44,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T00:00:00Z","timestamp":1736726400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>The study aimed to investigate the effects of <jats:italic>Chlorella vulgaris<\/jats:italic> and lysozyme on growth performance, diarrhea rate, immune function, plasma biochemical parameters, and gut microbiota and metabolites of weaned piglets.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Thirty weaned Xiangcun black piglets (BW, 11.47\u202f\u00b1\u202f1.13\u202fkg) were randomly assigned to one of three treatment groups: corn-soybean meal-based basal diet (CON group), soybean meal replaced with 5% <jats:italic>C. vulgaris<\/jats:italic> (CHV group), and soybean meal replaced with 5% <jats:italic>C. vulgaris<\/jats:italic> and 100\u202fmg\/kg lysozyme (LYSO group).<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Growth performance was not affected by <jats:italic>C. vulgaris<\/jats:italic> or <jats:italic>C. vulgaris<\/jats:italic> with lysozyme supplementation, while soybean meal partially replaced by <jats:italic>C. vulgaris<\/jats:italic> without lysozyme reduced the diarrhea rate of weaned piglets. Plasma biochemical analysis showed that plasma albumin, alkaline phosphatase, and high-density lipoprotein-cholesterol (HDL-C) levels in the CHV group and the total cholesterol and HDL-C levels in the LYSO group were higher when compared with the CON group. The LYSO group had increased interleukin (IL)-10 level in the jejunum and IL-1\u03b2 level in the ileum while having a decreasing IL-6 level in the jejunum of piglets. Additionally, although Firmicutes and <jats:italic>Megashaera_A<\/jats:italic> abundances and short-chain fatty acid concentrations (including acetate, propionate, butyrate, and valerate) were reduced in the CHV group, but several beneficial bacteria (such as Actinobacteroita, <jats:italic>Faecealibacterium,<\/jats:italic> and <jats:italic>Anaerovibrio<\/jats:italic>) abundances were increased in the LYSO group.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>In summary, dietary <jats:italic>C. vulgaris<\/jats:italic> or <jats:italic>C. vulgaris<\/jats:italic> with lysozyme supplementation improved health of piglets in some contexts without affecting growth performance. Therefore, soybean meal replaced by 5% <jats:italic>C. vulgaris<\/jats:italic> with or without lysozyme as sustainable feed ingredients in piglet diets could be a viable alternative approach.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fvets.2024.1505540","type":"journal-article","created":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T06:10:45Z","timestamp":1736748645000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":3,"title":["Effects of partial replacement of soybean meal with Chlorella vulgaris and lysozyme on diarrheal incidence, plasma biochemical parameters, and immunity of weaned piglets"],"prefix":"10.3389","volume":"11","author":[{"given":"Md. Abul Kalam","family":"Azad","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bowen","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ting","family":"Ye","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Binghua","family":"Qin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yordan","family":"Martinez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiangfeng","family":"Kong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,1,13]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"e34286","DOI":"10.7554\/eLife.34286","article-title":"Novel transgenic pigs with enhanced growth and reduced environmental impact","volume":"7","author":"Zhang","year":"2018","journal-title":"eLife"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/B978-0-323-99196-4.00039-5","article-title":"Microalgae application in feeds for monogastrics.","volume-title":"Handbook of food and feed from microalgae","author":"Costa","year":"2023"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/B978-0-12-821218-9.00009-8","article-title":"Microalgae as feed ingredients for livestock production and aquaculture.","volume-title":"Microalgae","author":"Valente","year":"2021"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"103545","DOI":"10.1016\/j.jff.2019.103545","article-title":"Microalgae\u2013nutritious, sustainable aqua- and animal feed source","volume":"62","author":"Dineshbabu","year":"2019","journal-title":"J Funct Foods"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.3390\/ani13061017","article-title":"Enhancing digestibility of Chlorella vulgaris biomass in monogastric diets: Strategies and insights","volume":"13","author":"Sp\u00ednola","year":"2023","journal-title":"Animals"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"2933","DOI":"10.3390\/foods10122933","article-title":"Using microalgae as a sustainable feed resource to enhance quality and nutritional value of pork and poultry meat","volume":"10","author":"Martins","year":"2021","journal-title":"Food Secur"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"5382","DOI":"10.1038\/s41598-019-41775-0","article-title":"Novel combination of feed enzymes to improve the degradation of Chlorella vulgaris recalcitrant cell wall","volume":"9","author":"Coelho","year":"2019","journal-title":"Sci Rep"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1111\/jpn.13470","article-title":"Effect of dietary inclusion of Spirulina on production performance, nutrient digestibility and meat quality traits in post-weaning piglets","volume":"105","author":"Martins","year":"2021","journal-title":"J Anim Physiol Anim Nutr"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"1155","DOI":"10.3390\/foods10061155","article-title":"Effects of Chlorella vulgaris as a feed ingredient on the quality and nutritional value of weaned piglets\u2019 meat","volume":"10","author":"Martins","year":"2021","journal-title":"Food Secur"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"1696","DOI":"10.1039\/c8fo02335b","article-title":"Dietary lysozyme supplementation contributes to enhanced intestinal functions and gut microflora of piglets","volume":"10","author":"Xiong","year":"2019","journal-title":"Food Funct"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1177\/0148607188012005465","article-title":"Effect of a fecal bulking agent on diarrhea during enteral feeding in the critically ill","volume":"12","author":"Hart","year":"1988","journal-title":"J Parenter Enteral Nutr"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"908753","DOI":"10.3389\/fimmu.2022.908753","article-title":"Dietary crude protein levels alter diarrhea incidence, immunity, and intestinal barrier function of Huanjiang mini-pigs during different growth stages","volume":"13","author":"Liu","year":"2022","journal-title":"Front Immunol"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"934890","DOI":"10.3389\/fmicb.2022.934890","article-title":"Probiotics or synbiotics addition to sows\u2019 diets alters colonic microbiome composition and metabolome profiles of offspring pigs","volume":"13","author":"Zhu","year":"2022","journal-title":"Front Microbiol"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"5837","DOI":"10.1039\/d1fo00208b","article-title":"Dietary supplementation with Bacillus subtilis and xylo-oligosaccharides improves growth performance and intestinal morphology and alters intestinal microbiota and metabolites in weaned piglets","volume":"12","author":"Ding","year":"2021","journal-title":"Food Funct"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.aninu.2023.07.009","article-title":"Amino acids in piglet diarrhea: Effects, mechanisms and insights","volume":"16","author":"Zhou","year":"2024","journal-title":"Anim Nutr"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1016\/j.aninu.2024.03.006","article-title":"Nutrition strategies to control post-weaning diarrhea of piglets: From the perspective of feeds","volume":"17","author":"Tang","year":"2024","journal-title":"Anim Nutr"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"6012","DOI":"10.1038\/s41598-022-10059-5","article-title":"Influence of Chlorella vulgaris on growth, digestibility and gut morphology and microbiota of weaned piglet","volume":"12","author":"Martins","year":"2022","journal-title":"Sci Rep"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1017\/S1751731116001543","article-title":"Effects of dietary supplementation with freshwater microalgae on growth performance, nutrient digestibility and gut health in weaned piglets","volume":"11","author":"Furbeyre","year":"2017","journal-title":"Animal"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"2264","DOI":"10.1017\/S1751731118000125","article-title":"Effects of oral supplementation with Spirulina and Chlorella on growth and digestive health in piglets around weaning","volume":"12","author":"Furbeyre","year":"2018","journal-title":"Animal"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"5910","DOI":"10.1039\/c9fo01456j","article-title":"Impact of sulfur-containing amino acids on the plasma metabolomics and intestinal microflora of the sow in late pregnancy","volume":"10","author":"Ding","year":"2019","journal-title":"Food Funct"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"1728","DOI":"10.1017\/S000711450999105X","article-title":"Effect of seaweed and cholesterol-enriched diets on postprandial lipoproteinaemia in rats","volume":"102","author":"Bocanegra","year":"2009","journal-title":"Br J Nutr"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"572","DOI":"10.3390\/md20090572","article-title":"A nutraceutical formulation containing brown algae reduces hepatic lipid accumulation by modulating lipid metabolism and inflammation in experimental models of NAFLD and NASH","volume":"20","author":"Gabbia","year":"2022","journal-title":"Mar Drugs"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"549","DOI":"10.3390\/ani14040549","article-title":"Nutritional and antioxidative benefits of dietary macroalgae supplementation in weaned piglets","volume":"14","author":"Czech","year":"2024","journal-title":"Animals"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1595","DOI":"10.3390\/ani13101595","article-title":"Dietary supplementation of Lactobacillus johnsonii Rs-7 improved antioxidant and immune function of weaned piglets","volume":"13","author":"Zhao","year":"2023","journal-title":"Animals"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"2617","DOI":"10.3390\/ani11092617","article-title":"Probiotics and Achyranthes bidentata polysaccharides improve growth performance via promoting intestinal nutrient utilization and enhancing immune function of weaned pigs","volume":"11","author":"Hou","year":"2021","journal-title":"Animals"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"16816","DOI":"10.1038\/s41598-022-21238-9","article-title":"Impact of dietary Chlorella vulgaris and feed enzymes on health status, immune response and liver metabolites in weaned piglets","volume":"12","author":"Martins","year":"2022","journal-title":"Sci Rep"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"8784","DOI":"10.1038\/s41598-023-36008-4","article-title":"Dietary Ulva lactuca and CAZyme supplementation improve serum biochemical profile and hepatic composition of weaned piglets","volume":"13","author":"Ribeiro","year":"2023","journal-title":"Sci Rep"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1038\/s41575-021-00472-y","article-title":"Dietary carbohydrates and fats in nonalcoholic fatty liver disease","volume":"18","author":"Yki-J\u00e4rvinen","year":"2021","journal-title":"Nat Rev Gastroenterol Hepatol"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"114922","DOI":"10.1016\/j.anifeedsci.2021.114922","article-title":"Effects of dietary carboxymethyl pachyman on oxidative stress and inflammation in weaned piglets challenged with diquat","volume":"276","author":"Azad","year":"2021","journal-title":"Anim Feed Sci Technol"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"628","DOI":"10.1038\/s41586-024-07098-5","article-title":"IL-10 constrains sphingolipid metabolism to limit inflammation","volume":"627","author":"York","year":"2024","journal-title":"Nature"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"1255533","DOI":"10.3389\/fimmu.2023.1255533","article-title":"Interleukin 6: At the interface of human health and disease","volume":"14","author":"Grebenciucova","year":"2023","journal-title":"Front Immunol"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"111","DOI":"10.3390\/cells10010111","article-title":"Cytokine-mediated crosstalk between immune cells and epithelial cells in the gut","volume":"10","author":"Mahapatro","year":"2021","journal-title":"Cells"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1017\/S1466252312000084","article-title":"The intestinal microbiome of the pig","volume":"13","author":"Isaacson","year":"2012","journal-title":"Anim Health Res Rev"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"338","DOI":"10.5713\/ab.21.0010","article-title":"Understanding intestinal health in nursery pigs and the relevant nutritional strategies","volume":"34","author":"Kim","year":"2021","journal-title":"Anim Biosci"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"859","DOI":"10.1152\/physrev.00045.2009","article-title":"Gut microbiota in health and disease","volume":"90","author":"Sekirov","year":"2010","journal-title":"Physiol Rev"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"18188","DOI":"10.1038\/s41598-024-68619-w","article-title":"Higher alpha diversity and Lactobacillus blooms are associated with better engraftment after fecal microbiota transplant in inflammatory bowel disease","volume":"14","author":"Zhang","year":"2024","journal-title":"Sci Rep"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"834598","DOI":"10.3389\/fvets.2022.834598","article-title":"Porcine models of the intestinal microbiota: The translational key to understanding how gut commensals contribute to gastrointestinal disease","volume":"9","author":"Rose","year":"2022","journal-title":"Front Vet Sci"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"2620","DOI":"10.3389\/fmicb.2019.02620","article-title":"Effect of fermented corn-soybean meal on serum immunity, the expression of genes related to gut immunity, gut microbiota, and bacterial metabolites in grower-finisher pigs","volume":"10","author":"Lu","year":"2019","journal-title":"Front Microbiol"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1186\/s40104-017-0216-y","article-title":"Alfalfa-containing diets alter luminal microbiota structure and short chain fatty acid sensing in the caecal mucosa of pigs","volume":"9","author":"Wang","year":"2018","journal-title":"J Anim Sci Biotechnol"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1002\/jobm.201100500","article-title":"Antibiotics production by an actinomycete isolated from the termite gut","volume":"52","author":"Matsui","year":"2012","journal-title":"J Basic Microbiol"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1186\/s40104-023-00958-6","article-title":"Dietary supplementation of benzoic acid and essential oils combination enhances intestinal resilience against LPS stimulation in weaned piglets","volume":"15","author":"Cui","year":"2024","journal-title":"J Anim Sci Biotechnol"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"100561","DOI":"10.1016\/j.animal.2022.100561","article-title":"Effect of dietary Bacillus coagulans on the performance and intestinal microbiota of weaned piglets","volume":"16","author":"Sun","year":"2022","journal-title":"Animal"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1186\/s12866-021-02143-z","article-title":"Effects of Clostridium butyricum on growth performance, metabonomics and intestinal microbial differences of weaned piglets","volume":"21","author":"Liang","year":"2021","journal-title":"BMC Microbiol"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"281","DOI":"10.3389\/fcimb.2018.00281","article-title":"Alterations in the abundance and co-occurrence of Akkermansia muciniphila and Faecalibacterium prausnitzii in the colonic mucosa of inflammatory bowel disease subjects","volume":"8","author":"Lopez-Siles","year":"2018","journal-title":"Front Cellul Infect Microbiol"}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2024.1505540\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T06:10:49Z","timestamp":1736748649000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2024.1505540\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,13]]},"references-count":44,"alternative-id":["10.3389\/fvets.2024.1505540"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2024.1505540","relation":{},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,13]]},"article-number":"1505540"}}