{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T04:01:38Z","timestamp":1788321698405,"version":"build-2803163510"},"reference-count":34,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2021,8,5]],"date-time":"2021-08-05T00:00:00Z","timestamp":1628121600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007605","name":"Aarhus Universitet","doi-asserted-by":"publisher","award":["CiFOOD"],"award-info":[{"award-number":["CiFOOD"]}],"id":[{"id":"10.13039\/100007605","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Foods"],"abstract":"<jats:p>Insects are suggested as a sustainable protein source of high nutritional quality, but the effects of insect ingestion on processes in the gastrointestinal tract and gut microbiota (GM) remain to be established. We examined the effects of partial substitution of meat with insect protein (Alphitobius diaperinus) in a four-week dietary intervention in a healthy rat model (n = 30). GM composition was characterized using\u2019 16S rRNA gene amplicon profiling while the metabolomes of stomach, small intestine, and colon content, feces and blood were investigated by 1H-NMR spectroscopy. Metabolomics analyses revealed a larger escape of protein residues into the colon and a different microbial metabolization pattern of aromatic amino acids when partly substituting pork with insect. Both for rats fed a pork diet and rats fed a diet with partial replacement of pork with insect, the GM was dominated by Lactobacillus, Clostridium cluster XI and Akkermansia. However, Bray-Curtis dissimilarity metrics were different when insects were included in the diet. Introduction of insects in a common Western omnivore diet alters the gut microbiome diversity with consequences for endogenous metabolism. This finding highlights the importance of assessing gastrointestinal tract effects when evaluating new protein sources as meat replacements.<\/jats:p>","DOI":"10.3390\/foods10081814","type":"journal-article","created":{"date-parts":[[2021,8,5]],"date-time":"2021-08-05T21:43:53Z","timestamp":1628199833000},"page":"1814","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Partial Substitution of Meat with Insect (Alphitobius diaperinus) in a Carnivore Diet Changes the Gut Microbiome and Metabolome of Healthy Rats"],"prefix":"10.3390","volume":"10","author":[{"given":"Sofie Kaas","family":"Lanng","sequence":"first","affiliation":[{"name":"Department of Food Science, Aarhus University, Agro Food Park 48, 8200 Aarhus, Denmark"},{"name":"CiFOOD, Centre for Innovative Food Research, Aarhus University, 8200 Aarhus, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yichang","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Food Science, University of Copenhagen, Rolighedsvej 30, 1958 Frederiksberg, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristine Rothaus","family":"Christensen","sequence":"additional","affiliation":[{"name":"Department of Veterinary and Animal Sciences, University of Copenhagen, Gr\u00f8nneg\u00e5rdsvej 15, 1958 Frederiksberg, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Axel Kornerup","family":"Hansen","sequence":"additional","affiliation":[{"name":"Department of Veterinary and Animal Sciences, University of Copenhagen, Gr\u00f8nneg\u00e5rdsvej 15, 1958 Frederiksberg, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8121-1114","authenticated-orcid":false,"given":"Dennis Sandris","family":"Nielsen","sequence":"additional","affiliation":[{"name":"Department of Food Science, University of Copenhagen, Rolighedsvej 30, 1958 Frederiksberg, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Witold","family":"Kot","sequence":"additional","affiliation":[{"name":"Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1882-5321","authenticated-orcid":false,"given":"Hanne Christine","family":"Bertram","sequence":"additional","affiliation":[{"name":"Department of Food Science, Aarhus University, Agro Food Park 48, 8200 Aarhus, Denmark"},{"name":"CiFOOD, Centre for Innovative Food Research, Aarhus University, 8200 Aarhus, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,8,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1126\/science.1257469","article-title":"World population stabilization unlikely this century","volume":"346","author":"Gerland","year":"2014","journal-title":"Science"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1126\/science.1185383","article-title":"Food security: The challenge of feeding 9 billion people","volume":"327","author":"Godfray","year":"2010","journal-title":"Science"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"6399","DOI":"10.1126\/science.aam5324","article-title":"Meat consumption, health, and the environment","volume":"361","author":"Godfray","year":"2018","journal-title":"Science"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s00394-019-01936-3","article-title":"Nutritional and health attributes of milk and milk imitations","volume":"59","author":"Ahrens","year":"2020","journal-title":"Eur. J. Nutr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1111\/1744-7917.12449","article-title":"Edible insects in China: Utilization and prospects","volume":"25","author":"Feng","year":"2018","journal-title":"Insect Sci."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Elhassan, M., Wendin, K., Olsson, V., and Langton, M. (2019). Quality Aspects of Insects as Food-Nutritional, Sensory, and Related Concepts. Foods, 8.","DOI":"10.3390\/foods8030095"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Oonincx, D.G., van Itterbeeck, J., Heetkamp, M.J., van den Brand, H., van Loon, J.J., and van Huis, A. (2010). An exploration on greenhouse gas and ammonia production by insect species suitable for animal or human consumption. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0014445"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1146\/annurev-ento-120811-153704","article-title":"Potential of Insects as Food and Feed in Assuring Food Security","volume":"58","author":"Huis","year":"2013","journal-title":"Annu. Rev. Entomol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1093\/nutrit\/nux057","article-title":"Consideration of insects as a source of dietary protein for human consumption","volume":"75","author":"Pinckaers","year":"2017","journal-title":"Nutr. Rev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1002\/mnfr.201200735","article-title":"Nutritional composition and safety aspects of edible insects","volume":"57","author":"Rumpold","year":"2013","journal-title":"Mol. Nutr. Food Res."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Fuso, A., Barbi, S., Macavei, L.I., Luparelli, A.V., Maistrello, L., Montorsi, M., Sforza, S., and Caligiani, A. (2021). Effect of the Rearing Substrate on Total Protein and Amino Acid Composition in Black Soldier Fly. Foods, 10.","DOI":"10.3390\/foods10081773"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Nyangena, D.N., Mutungi, C., Imathiu, S., Kinyuru, J., Affognon, H., Ekesi, S., Nakimbugwe, D., and Fiaboe, K.K.M. (2020). Effects of Traditional Processing Techniques on the Nutritional and Microbiological Quality of Four Edible Insect Species Used for Food and Feed in East Africa. Foods, 9.","DOI":"10.3390\/foods9050574"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Hermans, W.J.H., Senden, J.M., Churchward-Venne, T.A., Paulussen, K.J.M., Fuchs, C.J., Smeets, J.S.J., van Loon, J.J.A., Verdijk, L.B., and van Loon, L.J.C. (2021). Insects are a viable protein source for human consumption: From insect protein digestion to postprandial muscle protein synthesis in vivo in humans: A double-blind randomized trial. Am. J. Clin. Nutr.","DOI":"10.1093\/ajcn\/nqab115"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1093\/cdn\/nzaa049_044","article-title":"The Muscle Protein Synthetic Response Following Ingestion of Corn Protein, Milk Protein and Their Protein Blend in Young Males","volume":"4","author":"Pinckaers","year":"2020","journal-title":"Curr. Dev. Nutr."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Vangsoe, M.T., Joergensen, M.S., Heckmann, L.L., and Hansen, M. (2018). Effects of Insect Protein Supplementation during Resistance Training on Changes in Muscle Mass and Strength in Young Men. Nutrients, 10.","DOI":"10.3390\/nu10030335"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1186\/s40104-020-0425-7","article-title":"Comprehensive evaluation of the metabolic effects of insect meal from Tenebrio molitor L. in growing pigs by transcriptomics, metabolomics and lipidomics","volume":"11","author":"Meyer","year":"2020","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Vangsoe, M.T., Thogersen, R., Bertram, H.C., Heckmann, L.L., and Hansen, M. (2018). Ingestion of Insect Protein Isolate Enhances Blood Amino Acid Concentrations Similar to Soy Protein in A Human Trial. Nutrients, 10.","DOI":"10.3390\/nu10101357"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"10762","DOI":"10.1038\/s41598-018-29032-2","article-title":"Impact of Edible Cricket Consumption on Gut Microbiota in Healthy Adults, a Double-blind, Randomized Crossover Trial","volume":"8","author":"Stull","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"257","DOI":"10.3920\/JIFF2018.0048","article-title":"Nutritional evaluation of common (Tenebrio molitor) and lesser (Alphitobius diaperinus) mealworms in rats and processing effect on the lesser mealworm","volume":"5","author":"Jensen","year":"2019","journal-title":"J. Insects Food Feed."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1177\/0023677213516312","article-title":"FELASA recommendations for the health monitoring of mouse, rat, hamster, guinea pig and rabbit colonies in breeding and experimental units","volume":"48","author":"Berard","year":"2014","journal-title":"Lab. Anim."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.jmr.2009.11.012","article-title":"Icoshift: A versatile tool for the rapid alignment of 1D NMR spectra","volume":"202","author":"Savorani","year":"2010","journal-title":"J. Magn. Reson."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Rasmussen, T.S., de Vries, L., Kot, W., Hansen, L.H., Castro-Mej\u00eda, J.L., Vogensen, F.K., Hansen, A.K., and Nielsen, D.S. (2019). Mouse Vendor Influence on the Bacterial and Viral Gut Composition Exceeds the Effect of Diet. Viruses, 11.","DOI":"10.1101\/588160"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Edgar, R.C. (2016). UNOISE2: Improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv, 081257.","DOI":"10.1101\/081257"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Edgar, R.C. (2016). SINTAX: A simple non-Bayesian taxonomy classifier for 16S and ITS sequences. BioRxiv, 074161.","DOI":"10.1101\/074161"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"McMurdie, P.J., and Holmes, S. (2013). phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0061217"},{"key":"ref_26","unstructured":"Oksanen, J., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Peter, R., Minchin, R., O\u2019Hara, B., Gavin, L., and Simpson, P. (2019, January 01). Vegan: Community Ecology Package. Available online: http:\/\/CRAN.R-project.org\/package=vegan."},{"key":"ref_27","first-page":"27663","article-title":"Analysis of composition of microbiomes: A novel method for studying microbial composition","volume":"26","author":"Mandal","year":"2015","journal-title":"Microb. Ecol. Health Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2897","DOI":"10.3389\/fmicb.2018.02897","article-title":"Comparative Microbiome Signatures and Short-Chain Fatty Acids in Mouse, Rat, Non-human Primate, and Human Feces","volume":"9","author":"Nagpal","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"547","DOI":"10.3945\/ajcn.116.144428","article-title":"Metabolomic profiles as reliable biomarkers of dietary composition","volume":"105","author":"Esko","year":"2017","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1111\/j.1574-6941.1998.tb00487.x","article-title":"Enumeration of amino acid fermenting bacteria in the human large intestine: Effects of pH and starch on peptide metabolism and dissimilation of amino acids","volume":"25","author":"Smith","year":"1998","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Merz, B., Frommherz, L., Rist, M.J., Kulling, S.E., Bub, A., and Watzl, B. (2018). Dietary Pattern and Plasma BCAA-Variations in Healthy Men and Women-Results from the KarMeN Study. Nutrients, 10.","DOI":"10.3390\/nu10050623"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1900612","DOI":"10.1002\/mnfr.201900612","article-title":"Lower Circulating Branched-Chain Amino Acid Concentrations Among Vegetarians are Associated with Changes in Gut Microbial Composition and Function","volume":"63","author":"Wang","year":"2019","journal-title":"Mol. Nutr. Food Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1038\/nm.2307","article-title":"Metabolite profiles and the risk of developing diabetes","volume":"17","author":"Wang","year":"2011","journal-title":"Nat. Med."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/S0140-6736(18)31788-4","article-title":"Food in the Anthropocene: The EAT\u2013Lancet Commission on healthy diets from sustainable food systems","volume":"393","author":"Willett","year":"2019","journal-title":"Lancet"}],"container-title":["Foods"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2304-8158\/10\/8\/1814\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:41:18Z","timestamp":1760164878000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2304-8158\/10\/8\/1814"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,5]]},"references-count":34,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2021,8]]}},"alternative-id":["foods10081814"],"URL":"https:\/\/doi.org\/10.3390\/foods10081814","relation":{},"ISSN":["2304-8158"],"issn-type":[{"value":"2304-8158","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,5]]}}}