Bioactive compounds, antibiotics and heavy metals: Effects on the intestinal structure and microbiome of monogastric animals – a non-systematic review

Winiarska-Mieczan, Anna; Kwiecień, Małgorzata; Jachimowicz-Rogowska, Karolina; Muszyński, Siemowit; Tomaszewska, Ewa

doi:10.2478/aoas-2022-0057

Abstract

The intestinal structure and gut microbiota are essential for the animals’ health. Chemical components taken with food provide the right environment for a specific microbiome which, together with its metabolites and the products of digestion, create an environment, which in turn affects the population size of specific bacteria. Disturbances in the composition of the gut microbiota can be a reason for the malformation of guts, which has a decisive impact on the animal’s health. This review aimed to analyse scientific literature, published over the past 20 years, concerning the effect of nutritional factors on gut health, determined by the intestinal structure and microbiota of monogastric animals. Several topics have been investigated: bioactive compounds (probiotics, prebiotics, organic acids, and herbal active substances), antibiotics and heavy metals (essential minerals and toxic heavy metals).

References

Abdelli N., Pérez J.F., Vilarrasa E., Cabeza Luna I., Melo-Duran D., D’Angelo M., Solà-Oriol D. (2020). Targeted-release organic acids and essential oils improve performance and digestive function in broilers under a necrotic enteritis challenge. Animals, 10: 259.
Search in Google Scholar Back to article
Abu Hafsa S.H., Ibrahim S.A. (2018). Effect of dietary polyphenolrich grape seed on growth performance, antioxidant capacity and ileal microflora in broiler chicks. J. Anim. Physiol. Anim. Nutr., 102: 268–275.
Search in Google Scholar Back to article
Ali A., Ponnampalam E.N., Pushpakumara G., Cottrell J.J., Suleria H.A.R., Dunshea F.R. (2021). Cinnamon: A natural feed additive for poultry health and production – A review. Animals, 11: 2026.
Search in Google Scholar Back to article
Al-Mashhadani E.H., Al-Tememy S.A., Al-Jaff F.K., Al-Mashhadani H.E. (2013). Effect of supplementing broiler diet with anise and thyme essential oils on histological changes of small intestine. Egypt. Poult. Sci., 33: 249–259.
Search in Google Scholar Back to article
Al-Tarazi Y.H., Alshawabkeh K.M. (2003). Effect of dietary formic acid and propionic acids on Salmonella pullorum shedding and morality in layer chicks after experimental infection. J. Vet. Med. B., 50: 112–117.
Search in Google Scholar Back to article
An X., Bao Q., Di S., Zhao Y., Zhao S., Zhang H., Lian F., Tong X. (2019). The interaction between the gut microbiota and herbal medicines. Biomed. Pharmacother., 118: 109252.
Search in Google Scholar Back to article
Apajalahti J., Rademacher M., Htoo J., Redshaw M., Kettunen A. (2009). Divergent modulation of swine ileal microbiota by formic acid and methionine hydroxy analogue-free acid. Animal, 3: 817–825.
Search in Google Scholar Back to article
Arribas B., Suárez-Pereira E., Ortiz Mellet C., García Fernández J.M., Buttersack C., Rodríguez-Cabezas M.E., Garrido-Mesa N., Bailon E., Guerra-Hernández E., Zarzuelo A., Gálvez J. (2010). Di-D-fructose dianhydride-enriched caramels: effect on colon microbiota, inflammation, and tissue damage in trinitrobenzenesulfonic acid-induced colitic rats. J. Agric. Food Chem., 58: 6476–6484.
Search in Google Scholar Back to article
Arslan C., Pirinç A., Eker N., Sur E., Ündağ İ., Kuşat T. (2022). Dietary encapsulated essential oil mixture influence on apparent nutrient digestibility, serum metabolic profile, lymphocyte histochemistry and intestinal morphology of laying hens. Anim. Biosci., 35: 740–751.
Search in Google Scholar Back to article
Artym J., Zimecki M. (2020). Beneficial effect of lactoferrin on the microbiota from gastrointestinal tract. Adv. Microbiol., 59: 277–290.
Search in Google Scholar Back to article
Assefa S., Köhler G. (2020). Intestinal microbiome and metal toxicity. Curr. Opin. Toxicol., 19: 21–27.
Search in Google Scholar Back to article
Awad W.A., Ghareeb K., Abdel-Raheem S., Böhm J. (2009). Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poultry Sci., 88: 49–56.
Search in Google Scholar Back to article
Awad W.A., Ghareeb K., Böhm J. (2010). Effect of addition of a probiotic micro-organism to broiler diet on intestinal mucosal architecture and electrophysiological parameters. J. Anim. Physiol. Anim. Nutr., 94: 486–494.
Search in Google Scholar Back to article
Awad W.A., Ghareeb K., Böhm J. (2011). Evaluation of the chicory inulin efficacy on ameliorating the intestinal morphology and modulating the intestinal electrophysiological properties in broiler chickens. J. Anim. Physiol. Anim. Nutr., 95: 65–72.
Search in Google Scholar Back to article
Bansil R., Turner B.S. (2018). The biology of mucus: Composition, synthesis and organization. Adv. Drug Deliv. Rev., 124: 3–15.
Search in Google Scholar Back to article
Beasley D.E., Koltz A.M., Lambert J.E., Fierer N., Dunn R.R. (2015). The evolution of stomach acidity and its relevance to the human microbiome. PLOS One, 10: e0134116.
Search in Google Scholar Back to article
Bellido-Carreras N., Argüello H., Zaldívar-López S., Jiménez-Marín Á., Martins R.P., Arce C., Morera L., Carvajal A., Garrido J.J. (2019). Salmonella typhimurium infection along the porcine gastrointestinal tract and associated lymphoid tissues. Vet. Pathol., 56: 681–690.
Search in Google Scholar Back to article
Bento M.H.L., Ouwehand A.C., Tiihonen K., Lahtinen S., Nurminen P., Saarinen M.T., Schulze H., Mygind T., Fischer J. (2013). Essential oils and their use in animal feeds for monogastric animals – Effects on feed quality, gut microbiota, growth performance and food safety: A review. Vet. Med. (Czech), 58: 449–458.
Search in Google Scholar Back to article
Bist P., Choudhary S. (2022). Impact of heavy metal toxicity on the gut microbiota and its relationship with metabolites and future probiotics strategy: a review. Biol. Trace Elem. Res., https://doi.org/10.1007/s12011-021-03092-4 (online ahead of print).
Search in Google Scholar Back to article
Blank R., Sauer W.C., Mosenthin R., Zentek J., Huang S., Roth S. (2001). Effect of fumaric acid supplementation and dietary buffering capacity on the concentration of microbial metabolites in ileal digesta of young pigs. Can. J. Anim. Sci., 81: 345–353.
Search in Google Scholar Back to article
Bogusławska-Tryk M., Ziółkowska E., Sławińska A., Siwek M., Bogucka J. (2021). Modulation of intestinal histology by probiotics, prebiotics and synbiotics delivered in ovo in distinct chicken genotypes. Animals, 11: 3293.
Search in Google Scholar Back to article
Bolan S.S., Seshadri B., Keely S., Kunhikrishnan A., Bruce J., Grainge I., Talley N.J., Naidu R. (2021). Bioavailability of arsenic, cadmium, lead and mercury as measured by intestinal permeability. Sci. Rep., 11: 14675.
Search in Google Scholar Back to article
Borewicz K.A., Kim H.B., Singer R.S., Gebhart C.J., Sreevatsan S., Johnson T., Isaacson R.E. (2015). Changes in the porcine intestinal microbiome in response to infection with Salmonella enterica and Lawsonia intracellularis. PLOS One, 10(10): e0139106.
Search in Google Scholar Back to article
Breton J., Daniel C., Dewulf J., Pothion S., Froux N., Sauty M., Thomas P., Pot B., Foligné B. (2013 a). Gut microbiota limits heavy metals burden caused by chronic oral exposure. Toxicol. Lett., 222: 132–138.
Search in Google Scholar Back to article
Breton J., Le Clère K., Daniel C., Sauty M., Nakab L., Chassat T., Dewulf J., Penet S., Carnoy C., Thomas P., Pot B., Nesslany F., Foligné B. (2013 b). Chronic ingestion of cadmium and lead alters the bioavailability of essential and heavy metals, gene expression pathways and genotoxicity in mouse intestine. Arch. Toxicol., 87: 1787–1795.
Search in Google Scholar Back to article
Breton J., Massart S., Vandamme P., De Brandt E., Pot B., Foligné B. (2013 c) Ecotoxicology inside the gut: impact of heavy metals on the mouse microbiome. BMC Pharmacol. Toxicol., 14: 62.
Search in Google Scholar Back to article
Broom L. (2017). Necrotic enteritis; current knowledge and diet-related mitigation. Worlds Poult. Sci. J., 73: 281–292.
Search in Google Scholar Back to article
Calatayud M., Vélez D., Devesa V. (2012). Metabolism of inorganic arsenic in intestinal epithelial cell lines. Chem. Res. Toxicol., 25: 2402–2411.
Search in Google Scholar Back to article
Callejón-Leblic B., Selma-Royo M., Collado M.C., Abril N., García-Barrera T. (2021). Impact of antibiotic-induced depletion of gut microbiota and selenium supplementation on plasma selenoproteome and metal homeostasis in a mice model. J. Agric. Food Chem., 69: 7652–7662.
Search in Google Scholar Back to article
Callejón-Leblic B., Selma-Royo M., Collado M.C., Gómez-Ariza J.L., Abril N., García-Barrera T. (2022). Untargeted gut metabolomics to delve the interplay between selenium supplementation and gut microbiota. J. Proteome Res., 21: 758–767.
Search in Google Scholar Back to article
Caly D.L., D’lnca R., Auclair E., Drider D. (2015). Alternatives to antibiotics to prevent necrotic enteritis in broiler chickens: A microbiologist’s perspective. Front. Microbiol., 6: 1336.
Search in Google Scholar Back to article
Canibe N., Højberg O., Højsgaard S., Jensen B.B. (2005). Feed physical form and formic acid addition to the feed affect the gastrointestinal ecology and growth performance of growing pigs. J. Anim. Sci., 83: 1287–1302.
Search in Google Scholar Back to article
Cao G., Tao F., Hu Y., Li Z., Zhang Y., Deng B., Zhan X. (2019). Positive effects of a Clostridium butyricum-based compound probiotic on growth performance, immune responses, intestinal morphology, hypothalamic neurotransmitters, and colonic microbiota in weaned piglets. Food Funct., 10: 2926–2934.
Search in Google Scholar Back to article
Casas G.A., Blavi L., Cross T.L., Lee A.H., Swanson K.S., Stein H.H. (2020). Inclusion of the direct-fed microbial Clostridium butyricum in diets for weanling pigs increases growth performance and tends to increase villus height and crypt depth, but does not change intestinal microbial abundance. J. Anim. Sci., 98: skz372.
Search in Google Scholar Back to article
Chen J., Xie H., Chen D., Yu B., Mao X., Zheng P., Yu J., Luo Y., Luo J., He J. (2018). Chlorogenic acid improves intestinal development via suppressing mucosa inflammation and cell apoptosis in weaned pigs. ACS Omega, 3: 2211–2219.
Search in Google Scholar Back to article
Chen Y., Ni J., Li H. (2019). Effect of green tea and mulberry leaf powders on the gut microbiota of chicken. BMC Vet Res., 15: 77.
Search in Google Scholar Back to article
Chen S., Luo S., Yan C. (2022). Gut microbiota implications for health and welfare in farm animals: A review. Animals, 12: 93.
Search in Google Scholar Back to article
Cheng D., Li H., Zhou J., Wang S. (2019). Chlorogenic acid relieves lead-induced cognitive impairments and hepato-renal damage: via regulating the dysbiosis of the gut microbiota in mice. Food Funct., 10: 681–690.
Search in Google Scholar Back to article
Cheng S., Mao H., Ruan Y., Wu C., Xu Z., Hu G., Guo X., Zhang C., Cao H., Liu P. (2020). Copper changes intestinal microbiota of the cecum and rectum in female mice by 16S rRNA gene sequencing. Biol. Trace Elem. Res., 193: 445–455.
Search in Google Scholar Back to article
Chi L., Bian X., Gao B., Ru H., Tu P., Lu K. (2016). Sex-specific effects of arsenic exposure on the trajectory and function of the gut microbiome. Chem. Res. Toxicol., 29: 949–951.
Search in Google Scholar Back to article
Chi L., Bian X., Gao B., Tu P., Ru H., Lu K. (2017 a). The effects of an environmentally relevant level of arsenic on the gut microbiome and its functional metagenome. Toxicol. Sci., 160: 193–204.
Search in Google Scholar Back to article
Chi L., Gao B., Bian X., Tu P., Ru H., Lu K. (2017 b). Manganeseinduced sex-specific gut microbiome perturbations in C57BL/6 mice. Toxicol. Appl. Pharmacol., 331:142–153.
Search in Google Scholar Back to article
Chiocchetti G.M., Vélez D., Devesa V. (2018). Effect of subchronic exposure to inorganic arsenic on the structure and function of the intestinal epithelium. Toxicol. Lett., 286: 80–88.
Search in Google Scholar Back to article
Chiocchetti G.M., Vélez D., Devesa V. (2019). Inorganic arsenic causes intestinal barrier disruption. Metallomics, 11: 1411–1418.
Search in Google Scholar Back to article
Choi J.H., Lee K., Kim D.W., Kil D.Y., Kim G.B., Cha C.J. (2018). Influence of dietary avilamycin on ileal and cecal microbiota in broiler chickens. Poult. Sci., 97: 970–979.
Search in Google Scholar Back to article
Corfield A.P., Myerscough N., Longman R., Sylvester P., Arul S., Pignatelli M. (2000). Mucins and mucosal protection in the gastrointestinal tract: new prospects for mucins in the pathology of gastrointestinal disease. Gut, 47: 589–594.
Search in Google Scholar Back to article
Dai J., Yang X., Yuan Y., Jia Y., Liu G., Lin N., Xiao H., Zhang L., Chen J. (2020). Toxicity, gut microbiota and metabolome effects after copper exposure during early life in SD rats. Toxicology, 433–434: 152395.
Search in Google Scholar Back to article
Daisley B.A., Monachese M., Trinder M., Bisanz J.E., Chmiel J.A., Burton J.P., Reid G. (2019). Immobilization of cadmium and lead by Lactobacillus rhamnosus GR-1 mitigates apical-to-basolateral heavy metal translocation in a Caco-2 model of the intestinal epithelium. Gut Microbes., 10: 321–333.
Search in Google Scholar Back to article
Da Silva C.A., Bentin L.A.T., Dias C.P., Callegari M.A., Facina V.B., Dias F.T.F., Passos A., da Silva Martins C.C., Costa M.C. (2021). Impact of zinc oxide, benzoic acid and probiotics on the performance and cecal microbiota of piglets. Anim. Microbiome, 3: 86.
Search in Google Scholar Back to article
Dehghani N., Afsharmanesh M., Salarmoini M., Ebrahimnejad, H., Bitaraf A. (2018). Effect of pennyroyal, savory and thyme essential oils on Japanese quail physiology. Heliyon, 4: e00881.
Search in Google Scholar Back to article
Dela Cruz P.J.D., Dagaas C.T., Mangubat K.M.M., Angeles A.A., Abanto O.D. (2019). Dietary effects of commercial probiotics on growth performance, digestibility, and intestinal morphometry of broiler chickens. Trop. Anim. Health Prod., 51: 1105–1115.
Search in Google Scholar Back to article
Devi P.C., Samanta A.K., Das B., Kalita G., Behera P.S., Barman S. (2018). Effect of plant extracts and essential oil blend as alternatives to antibiotic growth promoters on growth performance, nutrient utilization and carcass characteristics of broiler chicken. Indian J. Anim. Nutri., 35: 421–427.
Search in Google Scholar Back to article
Dheer R., Patterson J., Dudash M., Stachler E.N., Bibby K.J., Stolz D.B., Shiva S., Wang Z., Hazen S.L., Barchowsky A., Stolz J.F. (2015). Arsenic induces structural and compositional colonic microbiome change and promotes host nitrogen and amino acid metabolism. Toxicol. Appl. Pharmacol., 289: 397–408.
Search in Google Scholar Back to article
Di Giancamillo A., Vitari F., Savoini G., Bontempo V., Bersani C., Dell’Orto V., Domeneghini C. (2008). Effects of orally administered probiotic Pediococcus acidilactici on the small and large intestine of weaning piglets. A qualitative and quantitative microanatomical study. Histol. Histopathol., 23: 651–664.
Search in Google Scholar Back to article
Diaz Carrasco J.M., Casanova N.A., Fernández Miyakawa M.E. (2019). Microbiota, gut health and chicken productivity: what is the connection? Microorganisms, 7: 374.
Search in Google Scholar Back to article
Dibner J.J., Buttin P. (2002). Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. J. Appl. Poult. Res., 11: 453–463.
Search in Google Scholar Back to article
Dobrowolski P., Muszyński S., Donaldson J., Jakubczak A., Żmuda A., Taszkun I., Rycerz K., Mielnik-Błaszczak M., Kuc D., Tomaszewska E. (2021). The effect of supplementation with β-hydroxy-β-methylbutyric acid (HMB) to pregnant sows on the mucosal structure, expression of intestinal barrier proteins and immunolocalization of VIP and leptin in the large intestine in their offspring. Animals, 11: 1468.
Search in Google Scholar Back to article
Dostal A., Fehlbaum S., Chassard C., Zimmermann M.B., Lacroix C. (2013). Low iron availability in continuous in vitro colonic fermentations induces strong dysbiosis of the child gut microbial consortium and a decrease in main metabolites. FEMS Microbiol. Ecol., 83: 161–175.
Search in Google Scholar Back to article
Dostal A., Lacroix C., Pham V.T., Zimmermann M.B., Del’homme C., Bernalier-Donadille A., Chassard C. (2014). Iron supplementation promotes gut microbiota metabolic activity but not colitis markers in human gut microbiota-associated rats. Br. J. Nutr., 111: 2135–2145.
Search in Google Scholar Back to article
Dostal A., Lacroix C., Bircher L., Pham V.T., Follador R., Zimmermann M.B., Chassard C. (2015). Iron modulates butyrate production by a child gut microbiota in vitro. mBio., 6: e01453-15.
Search in Google Scholar Back to article
Emge J.R., Huynh K., Miller E.N., Kaur M., Reardon C., Barrett K.E., Gareau M.G. (2016). Modulation of the microbiota-gut-brain axis by probiotics in a murine model of inflammatory bowel disease. Am. J. Physiol. Gastrointest. Liver Physiol., 310: 989–998.
Search in Google Scholar Back to article
Fujisawa H., Watanabe K., Suma K., Origuchi K., Matsufuji H., Seki T., Ariga T. (2009). Antibacterial potential of garlic-derived allicin and its cancellation by sulfhydryl compounds. Biosci. Biotechnol. Biochem., 73: 1948–1955.
Search in Google Scholar Back to article
Gabay O., Vicenty J., Smith D., Tiffany L., Ascher J., Curry T., Dennis J., Clouse K.A. (2020). Using a model of germ-free animals to study the impact of gut microbiome in research: a step by step sterility setting and management. Methods Protoc., 3: 18.
Search in Google Scholar Back to article
Gao B., Chi L., Mahbub R., Bian X., Tu P., Ru H., Lu K. (2017). Multiomics reveals that lead exposure disturbs gut microbiome development, key metabolites, and metabolic pathways. Chem. Res. Toxicol., 30: 9961005.
Search in Google Scholar Back to article
Ghazanfari S., Mohammadi Z., Adib Moradi M. (2015). Effects of coriander essential oil on the performance, blood characteristics, intestinal microbiota and histological of broilers. Braz. J. Poult. Sci., 17: 419–426.
Search in Google Scholar Back to article
Giambò F., Italia S., Teodoro M., Briguglio G., Furnari N., Catanoso R., Costa C., Fenga C. (2021). Influence of toxic metal exposure on the gut microbiota (review). World Acad. Sci. J., 3: 19.
Search in Google Scholar Back to article
Gokulan K., Arnold M.G., Jensen J., Vanlandingham M., Twaddle N.C., Doerge D.R., Cerniglia C.E., Khare S. (2018). Exposure to arsenite in CD-1 mice during juvenile and adult stages: effects on intestinal microbiota and gut-associated immune status. mBio., 9: e01418-18.
Search in Google Scholar Back to article
Grecco H.A.T., Amorim A.B., Saleh M.A.D., Tse M., Telles F.G., Miassi G.M., Pimenta G.M., Berto D.A. (2018). Evaluation of growth performance and gastro-intestinal parameters on the response of weaned piglets to dietary organic acids. An. Acad. Bras. Cienc., 90: 401–414.
Search in Google Scholar Back to article
Gülcin I., Huyut Z., Elmastas M., Aboul-Enein H.Y. (2010). Radical scavenging and antioxidant activity of tannic acid. Arab. J. Chem., 3: 43–53.
Search in Google Scholar Back to article
Guo X., Liu S., Wang Z., Zhang X.X., Li M., Wu B. (2014). Metagenomic profiles and antibiotic resistance genes in gut microbiota of mice exposed to arsenic and iron. Chemosphere, 112: 1–8.
Search in Google Scholar Back to article
Hanczakowska E., Świątkiewicz M. (2012). Effect of herbal extracts on piglet performance and small intestinal epithelial villi. Czech J. Anim. Sci., 57: 420–429.
Search in Google Scholar Back to article
Hassan Z.A., Zauszkiewicz-Pawlak A., Abdelrahman S.A., Algaidi S., Desouky M., Shalaby S.M. (2017). Morphological alterations in the jejunal mucosa of aged rats and the possible protective role of green tea. Folia Histochem. Cytobiol., 55: 124–139.
Search in Google Scholar Back to article
Herath M., Hosie S., Bornstein J.C., Franks A.E., Hill-Yardin E.L. (2020). The role of the gastrointestinal mucus system in intestinal homeostasis: implications for neurological disorders. Front. Cell. Infect. Microbiol., 10: 248.
Search in Google Scholar Back to article
Hernández F., García V., Madrid J., Orengo J., Catalá P., Megías M.D. (2006). Effect of formic acid on performance, digestibility, intestinal histomorphology and plasma metabolite levels of broiler chickens. Br. Poult. Sci., 47(1): 50–56.
Search in Google Scholar Back to article
Hoentjen F., Welling G.W., Harmsen H.J., Zhang X., Snart J., Tannock G.W., Lien K., Churchill T.A., Lupicki M., Dieleman L.A. (2005). Reduction of colitis by prebiotics in HLA-B27 transgenic rats is associated with microflora changes and immunomodulation. Inflamm. Bowel Dis., 11: 977–985.
Search in Google Scholar Back to article
Hosseinzadeh H., Alaw Qotbi A.A., Seidavi A., Norris D., Brown D. (2014). Effects of different levels of coriander (Coriandrum sativum) seed powder and extract on serum biochemical parameters, microbiota, and immunity in broiler chicks. Sci. World J., 2014: 628979.
Search in Google Scholar Back to article
Hrdina J., Banning A., Kipp A., Loh G., Blaut M., Brigelius-Flohé R. (2009). The gastrointestinal microbiota affects the selenium status and selenoprotein expression in mice. J. Nutr. Biochem., 20: 638–648.
Search in Google Scholar Back to article
Huang C., Shi Y., Zhou C., Guo L., Liu G., Zhuang Y., Li G., Hu G., Liu P., Guo X. (2021). Effects of subchronic copper poisoning on cecal histology and its microflora in chickens. Front. Microbiol., 12: 739577.
Search in Google Scholar Back to article
Jamroz D., Wiliczkiewicz A., Wertelecki T., Orda J., Skorupińska J. (2005). Use of active substances of plant origin in chicken diets based on maize and locally grown cereals. Br. Poult. Sci., 46: 485–493.
Search in Google Scholar Back to article
Jiang X., Gu S., Liu D., Zhao L., Xia S., He X., Chen H., Ge J. (2018). Lactobacillus brevis 23017 relieves mercury toxicity in the colon by modulation of oxidative stress and inflammation through the interplay of MAPK and NF-κB signaling cascades. Front. Microbiol., 9: 2425.
Search in Google Scholar Back to article
Jiao L., Lin F., Cao S., Wang C., Wu H., Shu M., Hu C. (2017). Preparation, characterization, antimicrobial and cytotoxicity studies of copper/zinc-loaded montmorillonite. J. Anim. Sci., 8: 27.
Search in Google Scholar Back to article
Johny A.K., Darre M., Donoghue A., Donoghue D., Venkitanarayanan K. (2010). Antibacterial effect of trans-cinnamaldehyde, eugenol, carvacrol, and thymol on Salmonella enteritidis and Campylobacter jejuni in chicken cecal contents in vitro. J. Appl. Poult. Res., 19: 237–244.
Search in Google Scholar Back to article
Kaczmarek B. (2020). Tannic acid with antiviral and antibacterial activity as a promising component of biomaterials – A minireview. Materials, 13: 3224.
Search in Google Scholar Back to article
Kalita A., Talukdar M., Sarma K., Kalita P.C., Roychoudhury P., Kalita G., Choudhary O.P., Chaudhary J.K., Doley P.J., Debroy S. (2021). Small intestinal mucosal cells in piglets fed with probiotic and zinc: a qualitative and quantitative microanatomical study. Folia Morphol. (Warsz), 80: 605–617.
Search in Google Scholar Back to article
Klebaniuk R., Tomaszewska E., Dobrowolski P., Kwiecień M., Burmańczuk A., Yanovych D., Zasadna Z., Szymańczyk S. E., Burmańczuk N., Muszyński S. (2018). Chloramphenicol-induced alterations in the liver and small intestine epithelium in pigs. Ann. Anim. Sci., 18: 429–440.
Search in Google Scholar Back to article
Kluge H., Broz J., Eder K. (2006). Effect of benzoic acid on growth performance, nutrient digestibility, nitrogen balance, gastrointestinal microflora and parameters of microbial metabolism in piglets. J. Anim. Physiol. Anim. Nutr., 90: 316–324.
Search in Google Scholar Back to article
Kociova S., Dolezelikova K., Horky P., Skalickova S., Baholet D., Bozdechova L., Vaclavkova E., Belkova J., Nevrkla P., Skladanka J., Do T., Zitka O., Haddad Y., Kopel P., Zurek L., Adam V., Smerkova K. (2020). Zinc phosphate-based nanoparticles as alternatives to zinc oxide in diet of weaned piglets. J. Anim. Sci. Biotechnol., 11: 59.
Search in Google Scholar Back to article
Koleva P., Ketabi A., Valcheva R., Gänzle M.G., Dieleman L.A. (2014). Chemically defined diet alters the protective properties of fructo-oligosaccharides and isomalto-oligosaccharides in HLAB27 transgenic rats. PLOS One, 9(11): e111717.
Search in Google Scholar Back to article
Koren O., Tako E. (2020). Chronic dietary zinc deficiency alters gut microbiota composition and function. Proceedings, 61: 16.
Search in Google Scholar Back to article
Kou H., Fua Y., Hea Y., Jianga J., Gaob X., Zhao H. (2019). Chronic lead exposure induces histopathological damage, microbiota dysbiosis and immune disorder in the cecum of female Japanese quails (Coturnix japonica). Ecotoxicol. Environ. Saf., 183: 109588.
Search in Google Scholar Back to article
La-ongkhum O., Pungsungvorn N., Amornthewaphat N., Nitisinprasert S. (2011). Effect of the antibiotic avilamycin on the structure of the microbial community in the jejunal intestinal tract of broiler chickens. Poultry Sci., 90: 1532–1538.
Search in Google Scholar Back to article
Lara-Villoslada F., de Haro O., Camuesco D., Comalada M., Velasco J., Zarzuelo A., Xaus J., Galvez J. (2006). Short-chain fructooligosaccharides, in spite of being fermented in the upper part of the large intestine, have anti-inflammatory activity in the TNBS model of colitis. Eur. J. Nutr., 45: 418–425.
Search in Google Scholar Back to article
Larsen I.S., Jensen B.A.H., Bonazzi E., Choi B.S.Y., Kristensen N.N., Schmidt E.G.W., Süenderhauf A., Morin L., Olsen P.B., Hansen L.B.S., Schröder T., Sina C., Chassaing B., Marette A. (2021). Fungal lysozyme leverages the gut microbiota to curb DSS-induced colitis. Gut Microbes., 13: 1988836.
Search in Google Scholar Back to article
Lazar V., Ditu L.M., Pircalabioru G.G., Gheorghe I., Curutiu C., Holban A.M., Picu A., Petcu L., Chifiriuc M.C. (2018). Aspects of gut microbiota and immune system interactions in infectious diseases, immunopathology, and cancer. Front. Immunol., 9: 1830.
Search in Google Scholar Back to article
Lee K.W., Lillehoj H.S. (2022). Role of Clostridium perfringens necrotic enteritis B-like toxin in disease pathogenesis. Vaccines, 10: 61.
Search in Google Scholar Back to article
Lei X., Piao X., Ru Y., Zhang H., Péron A., Zhang H. (2015). Effect of Bacillus amyloliquefaciens-based direct-fed microbial on performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. Asian-Australas. J. Anim. Sci., 28: 239–246.
Search in Google Scholar Back to article
Leung H., Yitbarek A., Snyder R., Patterson R., Barta J.R., Karrow N., Kiarie E. (2018). Responses of broiler chickens to Eimeria challenge when fed a nucleotide-rich yeast extract. Poultry Sci., 98: 1622–1633.
Search in Google Scholar Back to article
Levkut M., Fukasová M., Bobíková K., Levkutová M., Čobanová K., Levkut M. (2017). The effect of inorganic or organic zinc on the morphology of the intestine in broiler chickens. Folia Vet., 61: 52–56.
Search in Google Scholar Back to article
Li B.T., Van Kessel A.G., Caine W.R., Huang S.X., Kirkwood R.N. (2001). Small intestinal morphology and bacterial populations in ileal digesta and feces of newly weaned pigs receiving a high dietary level of zinc oxide. Can. J. Anim. Sci., 81: 511–516.
Search in Google Scholar Back to article
Li Y., Liu K., Shen J., Liu Y. (2016). Wheat bran intake can attenuate chronic cadmium toxicity in mice gut microbiota. Food Funct., 7: 3524–3530.
Search in Google Scholar Back to article
Li C.L., Wang J., Zhang H.J., Wu S.G., Hui Q.R., Yang C.B., Fang R.J., Qi G.H. (2019 a). Intestinal morphologic and microbiota responses to dietary Bacillus spp. in a broiler chicken model. Front. Physiol., 9: 1968.
Search in Google Scholar Back to article
Li X., Brejnrod A.D., Ernst M., Rykær M., Herschend J., Olsen N.M.C., Dorrestein P.C., Rensing C., Sørensen S.J. (2019 b). Heavy metal exposure causes changes in the metabolic health-associated gut microbiome and metabolites. Environ. Int., 126: 454–467.
Search in Google Scholar Back to article
Li A.L., Ni W.W., Zhang Q.M., Li Y., Zhang X., Wu H.Y., Du P., Hou J.C., Zhang Y. (2020). Effect of cinnamon essential oil on gut microbiota in the mouse model of dextran sodium sulfate-induced colitis. Microbiol. Immunol., 64: 23–32.
Search in Google Scholar Back to article
Li A., Ding J., Shen T., Han Z., Zhang J., Abadeen Z.U., Kulyar M.F., Wang X., Li K. (2021). Environmental hexavalent chromium exposure induces gut microbial dysbiosis in chickens. Ecotoxicol. Environ. Saf., 227: 112871.
Search in Google Scholar Back to article
Liu P., Piao X.S., Kim S.W., Wang L., Shen Y.B., Lee H.S., Li S.Y. (2008). Effects of chito-oligosaccharide supplementation on the growth performance, nutrient digestibility, intestinal morphology, and fecal shedding of Escherichia coli and Lactobacillus in weaning pigs. J. Anim. Sci., 86: 2609–2618.
Search in Google Scholar Back to article
Liu Y., Li Y., Liu K., Shen J. (2014). Exposing to cadmium stress cause profound toxic effect on microbiota of the mice intestinal tract. PLOS One, 9: e85323.
Search in Google Scholar Back to article
Liu L., Zeng D., Yang M., Wen B., Lai J., Zhou Y., Sun H., Xiong L., Wang J., Lin Y., Pan K., Jing B., Wang P., Ni X. (2019 a). Probiotic Clostridium butyricum Improves the growth performance, immune function, and gut microbiota of weaning rex rabbits. Probiotics Antimicrob. Proteins, 11: 1278–1292.
Search in Google Scholar Back to article
Liu Y., Ji J., Zhang W., Suo Y., Zhao J., Lin X., Cui L., Li B., Hu H., Chen C., Li Y.F. (2019 b). Selenium modulated gut flora and promoted decomposition of methylmercury in methylmercurypoisoned rats. Ecotoxicol. Environ. Saf., 185: 109720.
Search in Google Scholar Back to article
Liu L., Wu C., Chen D., Yu B., Huang Z., Luo Y., Zheng P., Mao X., Yu J., Luo J., Yan H., He J. (2020). Selenium-enriched yeast alleviates oxidative stress-induced intestinal mucosa disruption in weaned pigs. Oxid. Med. Cell. Longev., 2020: 5490743.
Search in Google Scholar Back to article
Liu W., Feng H., Zheng S., Xu S., Massey I.Y., Zhang C., Wang X., Yang F. (2021 a). Pb Toxicity on gut physiology and microbiota. Front. Physiol., 12: 574913.
Search in Google Scholar Back to article
Liu W., Rouzmehr F., Wang X., Seidavi A. (2021 b). Green tea dietary supplementation in broiler chickens: Effect on the development of chicken intestine. Food Sci. Nutr., 9: 1530–1541.
Search in Google Scholar Back to article
Liu X., Jin G., Tang Q., Huang S., Zhang Y., Sun Y., Liu T., Guo Z., Yang C., Wang B., Jiang K., Zhong W., Cao H. (2022). Early life Lactobacillus rhamnosus GG colonisation inhibits intestinal tumour formation. Br. J. Cancer, doi: 10.1038/s41416-021-01562-z. (online ahead of print).
Search in Google Scholar Back to article
Long L., Zhao X., Li H., Yan X., Zhang H. (2022). Effects of zinc lactate supplementation on growth performance, intestinal morphology, serum parameters, and hepatic metallothionein of chinese yellow-feathered broilers. Biol. Trace Elem. Res., 200: 1835–1843.
Search in Google Scholar Back to article
Lu K., Abo R.P., Schlieper K.A., Graffam M.E., Levine S., Wishnok J.S., Swenberg J.A., Tannenbaum S.R., Fox J.G. (2014). Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environ. Health Perspect., 122: 284–291.
Search in Google Scholar Back to article
Lückstädt C., Mellor S. (2011). The use of organic acids in animal nutrition, with special focus on dietary potassium diformate under European and Austral-Asian conditions. Recent Adv. Anim. Nutr. Aust., 18: 123–130.
Search in Google Scholar Back to article
Luczynski P., McVey Neufeld K.A., Oriach C.S., Clarke G., Dinan T.G., Cryan J.F. (2016). Growing up in a bubble: using germ-free animals to assess the influence of the gut microbiota on brain and behavior. Int. J. Neuropsychopharmacol., 19: pyw020.
Search in Google Scholar Back to article
Luise D., Motta V., Salvarani C., Chiappelli M., Fusco L.S., Bertocchi M., Mazzoni M., Maiorano G., Costa L.N., Milgen J.V., Bosi P., Trevisi P. (2017). Long-term administration of formic acid to weaners: Influence on intestinal microbiota, immunity parameters and growth performance. Anim. Feed. Sci. Technol., 232: 160–168.
Search in Google Scholar Back to article
Luise D., Correa F., Bosi P., Trevisi P. (2020). A review of the effect of formic acid and its salts on the gastrointestinal microbiota and performance of pigs. Animals, 10: 887.
Search in Google Scholar Back to article
Lukovac S., Belzer C., Pellis L., Keijser B.J., de Vos W.M., Montijn R.C., Roeselers G. (2014). Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. mBio., 5: e01438-14.
Search in Google Scholar Back to article
Luo J., Chen D., Mao X., He J., Yu B., Cheng L., Zeng D. (2019). Purified β-glucans of different molecular weights enhance growth performance of LPS-challenged piglets via improved gut barrier function and microbiota. Animals, 9: 602.
Search in Google Scholar Back to article
Ma J., Piao X., Shang Q., Long S., Liu S., Mahfuz S. (2021). Mixed organic acids as an alternative to antibiotics improve serum biochemical parameters and intestinal health of weaned piglets. Anim. Nutr., 7: 737–749.
Search in Google Scholar Back to article
Madlala T., Okpeku M., Adeleke M.A. (2021). Understanding the interactions between Eimeria infection and gut microbiota, towards the control of chicken coccidiosis: a review. Parasite, 28: 48.
Search in Google Scholar Back to article
Mathew T.C., Abdeen S.M., Dashti H., Asfar S. (2017). Green tea induced cellular proliferation and the expression of transforming growth factor-β1 in the jejunal mucosa of fasting rats. Med. Princ. Pract., 26: 343–350.
Search in Google Scholar Back to article
Melhem H., Regan-Komito D., Niess J.H. (2021). Mucins dynamics in physiological and pathological conditions. Int. J. Mol. Sci., 22: 13642.
Search in Google Scholar Back to article
Mroz Z., Reese D.E., Øverland M., Van Diepen J.T.M., Kogut J. (2002). The effects of potassium diformate and its molecular constituents on the apparent ileal and fecal digestibility and retention of nutrients in growing-finishing pigs. J. Anim. Sci., 80: 681–690.
Search in Google Scholar Back to article
Muhammad A.I., Mohamed D.A., Chwen L.T., Akit H., Samsudin A.A. (2021). Effect of selenium sources on laying performance, egg quality characteristics, intestinal morphology, microbial population and digesta volatile fatty acids in laying hens. Animals, 11: 1681.
Search in Google Scholar Back to article
Müller A., Eller J., Albrecht F., Prochnow P., Kuhlmann K., Bandow J.E., Slusarenko A.J., Leichert L.I. (2016). Allicin induces thiol stress in bacteria through s-allylmercapto modification of protein cysteines. J. Biol. Chem., 291: 11477–11490.
Search in Google Scholar Back to article
Murai A., Kitahara K., Okumura S., Kobayashi M., Horio F. (2016). Oral antibiotics enhance antibody responses to keyhole limpet hemocyanin in orally but not muscularly immunized chickens. Anim. Sci. J., 87: 257–265.
Search in Google Scholar Back to article
Mustafa A., Bai S., Zeng Q., Ding X., Wang J., Xuan Y., Su Z., Zhang K. (2021). Effect of organic acids on growth performance, intestinal morphology, and immunity of broiler chickens with and without coccidial challenge. AMB Expr., 11: 140.
Search in Google Scholar Back to article
Nabian S., Arabkhazaeli F., Seifouri P., Farahani A. (2018). Morphometric analysis of the intestine in experimental coccidiosis in broilers treated with anticoccidial drugs. Iran J. Parasitol., 13: 493–499.
Search in Google Scholar Back to article
Namkung H., Li M., Gong J., Yu H., Cottrill M., de Lange C.F.M. (2004). Impact of feeding blends of organic acids and herbal extracts on growth performance, gut microbiota and digestive function in newly weaned pigs. Can. J. Anim. Sci., 84: 697–704.
Search in Google Scholar Back to article
Nielsen K.M., Zhang Y., Curran T.E., Magnuson J.T., Venables B.J., Durrer K.E., Allen M.S., Roberts A.P. (2018). Alterations to the intestinal microbiome and metabolome of Pimephales promelas and Mus musculus following exposure to dietary methylmercury. Environ. Sci. Technol., 52: 8774–8784.
Search in Google Scholar Back to article
Nwachukwu C.U., Aliyu K.I., Ewuola E.O. (2021). Growth indices, intestinal histomorphology, and blood profile of rabbits fed probiotics-and prebiotics-supplemented diets. Transl. Anim. Sci., 5: txab096.
Search in Google Scholar Back to article
Oakley B.B., Buhr R.J., Ritz C.W., Kiepper B.H., Berrang M.E., Seal B.S., Cox N.A. (2014). Successional changes in the chicken cecal Bioactive compounds, antibiotics and heavy metals in gut health 311 microbiome during 42 days of growth are independent of organic acid feed additives. BMC Vet. Res., 10: 282.
Search in Google Scholar Back to article
Oliver W.T., Wells J.E. (2013). Lysozyme as an alternative to antibiotics improves growth performance and small intestinal morphology in nursery pigs. J. Anim. Sci., 91: 3129–3136.
Search in Google Scholar Back to article
Pajarillo E., Lee E., Kang D.K. (2021). Trace metals and animal health: Interplay of the gut microbiota with iron, manganese, zinc, and copper. Anim. Nutr., 7: 750–761.
Search in Google Scholar Back to article
Palamidi I., Mountzouris K.C. (2018). Diet supplementation with an organic acids-based formulation affects gut microbiota and expression of gut barrier genes in broilers. Anim. Nutr., 4: 367–377.
Search in Google Scholar Back to article
Paone P., Cani P.D. (2020). Mucus barrier, mucins and gut microbiota: the expected slimy partners? Gut, 69: 2232–2243.
Search in Google Scholar Back to article
Pathak M., Mandal G.P., Patra A.K., Samanta I., Pradhan S., Haldar S. (2017). Effects of dietary supplementation of cinnamaldehyde and formic acid on growth performance, intestinal microbiota and immune response in broiler chickens. Anim. Prod. Sci., 57: 821–827.
Search in Google Scholar Back to article
Pei X., Xiao Z., Liu L., Wang G., Tao W., Wang M., Zou J., Leng D. (2019). Effects of dietary zinc oxide nanoparticles supplementation on growth performance, zinc status, intestinal morphology, microflora population, and immune response in weaned pigs. J. Sci. Food Agric., 99: 1366–1374.
Search in Google Scholar Back to article
Peng Z., Zhang J., Fanning S., Wang L., Li M., Maheshwari N., Sun J., Li F. (2019). Effects of metal and metalloid pollutants on the microbiota composition of feces obtained from twelve commercial pig farms across China. Sci. Total. Environ., 647: 577–586.
Search in Google Scholar Back to article
Petersen A., Bergström A., Andersen J.B., Hansen M., Lahtinen S.J., Wilcks A., Licht T.R. (2010). Analysis of the intestinal microbiota of oligosaccharide fed mice exhibiting reduced resistance to Salmonella infection. Benef. Microbes., 1: 271–281.
Search in Google Scholar Back to article
Pieper R., Vahjen W., Neumann K., Van Kessel A.G., Zentek J. (2012). Dose-dependent effects of dietary zinc oxide on bacterial communities and metabolic profiles in the ileum of weaned pigs. J. Anim. Physiol. Anim. Nutr., 96: 825–833.
Search in Google Scholar Back to article
Placha I., Simonova M.P., Cobanova K., Laukova A., Faix S. (2010). Effect of enterococcus faecium AL41 and Thymus vulgaris essential oil on small intestine integrity and antioxidative status of laying hens. Res. Vet. Sci., 89: 257–261.
Search in Google Scholar Back to article
Placha I., Chrastinova L., Laukova A., Cobanova K., Takacova J., Strompfova V., Chrenkova M., Formelova Z., Faix S. (2013). Effect of thyme oil on small intestine integrity and antioxidant status, phagocytic activity and gastrointestinal microbiota in rabbits. Acta Vet. Hung., 61: 197–208.
Search in Google Scholar Back to article
Placha I., Takacova J., Ryzner M., Cobanova K., Laukova A., Strompfova V., Venglovska K., Faix S. (2014). Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers. Br. Poult. Sci., 55: 105–114.
Search in Google Scholar Back to article
Pothuraju R., Chaudhary S., Rachagani S., Kaur S., Roy H.K., Bouvet M., Batra S.K. (2021). Mucins, gut microbiota, and postbiotics role in colorectal cancer. Gut Microbes., 13: 1974795.
Search in Google Scholar Back to article
Puvaca N., Milenković J., Galonja Coghill T., Bursić V., Petrović A., Tanasković S., Pelić M., Ljubojević Pelić D., Miljković T. (2021). Antimicrobial activity of selected essential oils against selected pathogenic bacteria: in vitro study. Antibiotics, 10: 546.
Search in Google Scholar Back to article
Qin H.L., Shen T.Y., Gao Z.G., Fan X.B., Hang X.M., Jiang Y.Q., Zhang H.Z. (2005). Effect of lactobacillus on the gut microflora and barrier function of the rats with abdominal infection. World J. Gastroenterol., 11: 2591–2596.
Search in Google Scholar Back to article
Radi Z.A. (2004). An epizootic of combined Clostridium perfringens, Eimeria spp. and Capillaria spp. enteritis and Histomonas spp. hepatitis with Escherichia coli septicemia in bobwhite quails (Colinus virginianus). Int. J. Poult. Sci., 3: 438–441.
Search in Google Scholar Back to article
Rashid Z., Mirani Z.A., Zehra S., Gilani S.M.H., Ashraf A., Azhar A., Al-Ghanim K.A., Al-Misned F., Al-Mulahim N., Mahboob S. (2020). Enhanced modulation of gut microbial dynamics affecting body weight in birds triggered by natural growth promoters administered in conventional feed. Saudi J. Biol. Sci., 27: 2747–2755.
Search in Google Scholar Back to article
Rastad A. (2020). Effects of antibiotic replacement with garlic powder and probiotic on performance, carcass characteristics, oxidative enzymes and intestinal morphology of broiler chickens. Acta Sci. Anim. Sci., 42: e48734.
Search in Google Scholar Back to article
Rebersek M. (2021). Gut microbiome and its role in colorectal cancer. BMC Cancer, 21: 1325.
Search in Google Scholar Back to article
Reed S., Knez M., Uzan A., Stangoulis J.C.R., Glahn R.P., Koren O., Tako E. (2018). Alterations in the gut (Gallus gallus) microbiota following the consumption of zinc biofortified wheat (Triticum aestivum)-based diet. J. Agric. Food Chem., 66: 6291–6299.
Search in Google Scholar Back to article
Ren H., Saliu E.M., Zentek J., Goodarzi Boroojeni F., Vahjen W. (2019). Screening of host specific lactic acid bacteria active against Escherichia coli from massive sample pools with a combination of in vitro and ex vivo methods. Front. Microbiol., 10: 2705.
Search in Google Scholar Back to article
Richardson J.B., Dancy B.C.R., Horton C.L., Lee Y.S., Madejczyk M.S., Xu Z.Z., Ackermann G., Humphrey G., Palacios G., Knight R., Lewis J.A. (2018). Exposure to toxic metals triggers unique responses from the rat gut microbiota. Sci. Rep., 8: 6578.
Search in Google Scholar Back to article
Ricke S.C., Dittoe D.K., Richardson K.E. (2020). Formic acid as an antimicrobial for poultry production: a review. Front. Vet. Sci., 7: 563.
Search in Google Scholar Back to article
Ruan Y., Wu C., Guo X., Xu Z., Xing C., Cao H., Zhang C., Hu G., Liu P. (2019). High doses of copper and mercury changed cecal microbiota in female mice. Biol. Trace Elem. Res., 189: 134–144.
Search in Google Scholar Back to article
Ruczizka U., Metzler-Zebeli B.U., Unterweger C., Mann E., Schwarz L., Knecht C., Hennig-Pauka I. (2019). Early parenteral administration of ceftiofur has gender-specific short- and long-term effects on the fecal microbiota and growth in pigs from the suckling to growing phase. Animals, 10: 17.
Search in Google Scholar Back to article
Ruzauskas M., Bartkiene E., Stankevicius A., Bernatoniene J., Zadeike D., Lele V., Starkute V., Zavistanaviciute P., Grigas J., Zokaityte E., Pautienius A., Juodeikiene G., Jakstas V. (2020). The influence of essential oils on gut microbial profiles in pigs. Animals, 10: 1734.
Search in Google Scholar Back to article
Sand J.M., Arendt M.K., Repasy A., Deniz G., Cook M.E. (2016). Oral antibody to interleukin-10 reduces growth rate depression due to Eimeria spp. infection in broiler chickens. Poult. Sci., 95: 439–446.
Search in Google Scholar Back to article
Schokker D., Zhang J., Zhang L.L., Vastenhouw S.A., Heilig H.G., Smidt H., Rebel J.M., Smits M.A. (2014). Early-life environmental variation affects intestinal microbiota and immune development in new-born piglets. PLOS One, 9(6): e100040.
Search in Google Scholar Back to article
Schokker D., Jansman A.J., Veninga G., de Bruin N., Vastenhouw S.A., de Bree F.M., Bossers A., Rebel J.M., Smits M.A. (2017). Perturbation of microbiota in one-day old broiler chickens with antibiotic for 24 hours negatively affects intestinal immune development. BMC Genomics, 18: 241.
Search in Google Scholar Back to article
Shannon M.C., Hill G.M. (2019). Trace mineral supplementation for the intestinal health of young monogastric animals. Front. Vet. Sci., 6: 73.
Search in Google Scholar Back to article
Shao X., Sun C., Tang X., Zhang X., Han D., Liang S., Qu R., Hui X., Shan Y., Hu L., Fang H., Zhang H., Wu X., Chen C. (2020). Anti-inflammatory and intestinal microbiota modulation properties of jinxiang garlic (Allium sativum L.) polysaccharides toward dextran sodium sulfate-induced colitis. J. Agric. Food Chem., 68: 12295–12309.
Search in Google Scholar Back to article
Shen Y.B., Piao X.S., Kim S.W., Wang L., Liu P., Yoon I., Zhen Y.G. (2009). Effects of yeast culture supplementation on growth performance, intestinal health, and immune response of nursery pigs. J. Anim. Sci., 87: 2614–2624.
Search in Google Scholar Back to article
Shen J., Chen Y., Wang Z., Zhou A., He M., Mao L., Zou H., Peng Q., Xue B., Wang L., Zhang X., Wu S., Lv Y. (2014). Coated zinc oxide improves intestinal immunity function and regulates microbiota composition in weaned piglets. Br. J. Nutr., 111: 2123–2134.
Search in Google Scholar Back to article
Shim S.B., Verstegen M.W., Kim I.H., Kwon O.S., Verdonk J.M. (2005). Effects of feeding antibiotic-free creep feed supplemented with oligofructose, probiotics or synbiotics to suckling piglets increases the preweaning weight gain and composition of intestinal microbiota. Arch. Anim. Nutr., 59: 419–427.
Search in Google Scholar Back to article
Shrivastava R., Kannan A., Upreti R.K., Chaturvedi U.C. (2005). Effects of chromium on the resident gut bacteria of rat. Toxicol. Mech. Methods, 15: 211–218.
Search in Google Scholar Back to article
Sieniawska E. (2015). Activities of tannins – from in vitro studies to clinical trials. Nat. Prod Commun., 10: 1877–1884.
Search in Google Scholar Back to article
Simon K., Verwoolde M.B., Zhang J., Smidt H., de Vries Reilingh G., Kemp B., Lammers A. (2016). Long-term effects of early life microbiota disturbance on adaptive immunity in laying hens. Poult. Sci., 95: 1543–1554.
Search in Google Scholar Back to article
Sivam G.P. (2001). Protection against Helicobacter pylori and other bacterial infections by garlic. J. Nutr., 131: 1106S–1108S.
Search in Google Scholar Back to article
Sizentsov A.N., Kvan O.V., Miroshnikova E.P., Gavrish I.A., Serdaeva V.A., Bykov A.V. (2018). Assessment of biotoxicity of Cu nanoparticles with respect to probiotic strains of microorganisms and representatives of the normal flora of the intestine of broiler chickens. Environ. Sci. Pollut. Res., 25: 15765–15773.
Search in Google Scholar Back to article
Smirnov A., Perez R., Amit-Romach E., Sklan D., Uni Z. (2005). Mucin dynamics and microbial populations in chicken small intestine are changed by dietary probiotic and antibiotic growth promoter supplementation. J. Nutr., 135: 187–192.
Search in Google Scholar Back to article
Song R., Yao J., Shi Q., Wei R. (2018). Nanocomposite of half-fin anchovy hydrolysates/zinc oxide nanoparticles exhibits actual non-toxicity and regulates intestinal microbiota, short-chain fatty acids production and oxidative status in mice. Mar. Drugs., 16: 23.
Search in Google Scholar Back to article
Tatara M.R., Śliwa E., Dudek K.A., Kowalik S., Gawron A., Piersiak T., Dobrowolski P., Studziński T. (2005 a). Effect of aged garlic extract and allicin administration to sows during pregnancy and lactation on body weight gain and gastrointestinal tract development of piglets: morphological properties of the small intestine. Part II. Bull. Vet. Inst. Pulawy, 49: 455–464.
Search in Google Scholar Back to article
Tatara M.R., Sliwa E., Dudek K., Mosiewicz J., Studzinski T. (2005 b). Effect of aged garlic extract and allicin administration to sows during pregnancy and lactation on body weight gain and gastrointestinal tract development of piglets. Part I. Bull. Vet. Inst. Pulawy, 49: 349–355.
Search in Google Scholar Back to article
Tatara M.R., Sliwa E., Dudek K., Gawron A., Piersiak T., Dobrowolski P., Mosiewicz J., Siwicki A., Studzinski T. (2008). Aged garlic extract and allicin improve performance and gastrointestinal tract development of piglets reared in artificial sow. Ann. Agric. Environ. Med., 15: 63–69.
Search in Google Scholar Back to article
Tharmaraj N., Shah N.P. (2009). Antimicrobial effects of probiotics against selected pathogenic and spoilage bacteria in cheese-based dips. Int. Food Res. J., 16: 261–276.
Search in Google Scholar Back to article
Tomaszewska E., Dobrowolski P., Puzio I. (2012). Postnatal administration of 2-oxoglutaric acid improves the intestinal barrier affected by the prenatal action of dexamethasone in pigs. Nutrition, 28: 190–196.
Search in Google Scholar Back to article
Tomaszewska E., Winiarska-Mieczan A., Dobrowolski P. (2015 a). Hematological and serum biochemical parameters of blood in adolescent rats and histomorphological changes in the jejunal epithelium and liver after chronic exposure to cadmium and lead in the case of supplementation with green tea vs black, red or white tea. Exp. Toxicol. Pathol., 67: 331–339.
Search in Google Scholar Back to article
Tomaszewska E., Winiarska-Mieczan A., Dobrowolski P. (2015 b). The lack of protective effects of tea supplementation on liver and jejunal epithelium in adult rats exposed to cadmium and lead. Environ. Toxicol. Pharmacol., 40: 708–714.
Search in Google Scholar Back to article
Tomaszewska E., Dobrowolski P., Kwiecień M. (2016). Intestinal alterations, basal hematology, and biochemical parameters in adolescent rats fed different sources of dietary copper. Biol. Trace Elem. Res., 171: 185–191.
Search in Google Scholar Back to article
Tomaszewska E., Dobrowolski P., Kwiecień M. (2017). Alterations in intestinal and liver histomorphology and basal hematological and biochemical parameters in relation to different sources of dietary copper in adult rats. Ann. Anim. Sci., 17: 477–490.
Search in Google Scholar Back to article
Tomaszewska E., Świątkiewicz S., Arczewska-Włosek A., Wojtysiak D., Dobrowolski P., Domaradzki P., Świetlicka I., Donaldson J., Hułas-Stasiak M., Muszyński S. (2020). Alpha-ketoglutarate: an effective feed supplement in improving bone metabolism and muscle quality of laying hens: a preliminary study. Animals, 10: 2420.
Search in Google Scholar Back to article
Tomaszewska E., Prost Ł., Dobrowolski P., Chand D.K.P., Donaldson J., Czech A., Klebanikuk R., Fabjanowska J., Muszyński S. (2022). Prenatal programming of the small intestine in piglets: the effect of supplementation with 3-hydroxy-3-methylbutyric acid (HMB) in pregnant sows on the structure of jejunum of their offspring. Ann. Anim. Sci., 22: 613–623.
Search in Google Scholar Back to article
Tomaszewska E., Dobrowolski P., Prost Ł., Chand D.K.P., Donaldson J., Winiarczyk D., Jarosz Ł., Ciszewski A., Czech A., Muszyński S. (2023). The effect of supplementation with β-hydroxy-β-methylbutyric acid (HMB) to pregnant sows on the mucosal structure, immunolocalization of intestinal barrier proteins, VIP and leptin in the large intestine in their offspring. Ann. Anim. Sci., 23: 87–96.
Search in Google Scholar Back to article
Tretola M., Maghin F., Silacci P., Ampuero S., Bee G. (2019). Effect of supplementing hydrolysable tannins to a grower-finisher diet containing divergent pufa levels on growth performance, boar taint levels in back fat and intestinal microbiota of entire males. Animals, 9: 1063.
Search in Google Scholar Back to article
Tsiouris V. (2016). Poultry management: A useful tool for the control of necrotic enteritis in poultry. Avian Pathol., 45: 323–325.
Search in Google Scholar Back to article
Uzal F.A., Freedman J.C., Shrestha A., Theoret J.R., Garcia J., Awad M.M., Adams V., Moore R.J., Rood J.I., McClane B.A. (2014). Towards an understanding of the role of Clostridium perfringens toxins in human and animal disease. Future Microbiol., 9: 361–377.
Search in Google Scholar Back to article
Valeriano V.D., Balolong M.P., Kang D.K. (2017). Probiotic roles of Lactobacillus sp. in swine: insights from gut microbiota. J. Appl. Microbiol., 122: 554–567.
Search in Google Scholar Back to article
van der Peet-Schwering C.M., Jansman A.J., Smidt H., Yoon I. (2007). Effects of yeast culture on performance, gut integrity, and blood cell composition of weanling pigs. J. Anim. Sci., 85: 3099–3109.
Search in Google Scholar Back to article
Van Immerseel F., Russell J.B., Flythe M.D., Gantois I., Timbermont L., Pasmans F., Haesebrouck F., Ducatelle R. (2006). The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy, Avian Pathol., 35: 182–188.
Search in Google Scholar Back to article
Van Noten N., Degroote J., Van Liefferinge E., Taminiau B., De Smet S., Desmet T., Michiels J. (2020). Effects of thymol and thymol α-D-Glucopyranoside on intestinal function and microbiota of weaned pigs. Animals, 10: 329.
Search in Google Scholar Back to article
Villagómez-Estrada S., Pérez J.F., Darwich L., Vidal A., van Kuijk S., Melo-Durán D., Solà-Oriol D. (2020). Effects of copper and zinc sources and inclusion levels of copper on weanling pig performance and intestinal microbiota. J. Anim. Sci., 98: skaa117.
Search in Google Scholar Back to article
Wang H., Ni X., Qing X., Zeng D., Luo M., Liu L., Li G., Pan K., Jing B. (2017 a). Live probiotic Lactobacillus johnsonii BS15 promotes growth performance and lowers fat deposition by improving lipid metabolism, intestinal development, and gut microflora in broilers. Front. Microbiol., 8: 1073.
Search in Google Scholar Back to article
Wang Y., Sun J., Zhong H., Li N., Xu H., Zhu Q., Liu Y. (2017 b). Effect of probiotics on the meat flavour and gut microbiota of chicken. Sci. Rep.,7: 6400.
Search in Google Scholar Back to article
Wang C., Cheng K., Zhou L., He J., Zheng X., Zhang L., Zhong X., Wang T. (2017 c). Evaluation of long-term toxicity of oral zinc oxide nanoparticles and zinc sulfate in mice. Biol. Trace Elem. Res., 178: 276–282.
Search in Google Scholar Back to article
Wang K., Cao G., Zhang H., Li Q., Yang C. (2019). Effects of Clostridium butyricum and Enterococcus faecalis on growth performance, immune function, intestinal morphology, volatile fatty acids, and intestinal flora in a piglet model. Food Funct., 10: 7844–7854.
Search in Google Scholar Back to article
Wang H., Zhang S., Yang F., Xin R., Wang S., Cui D., Sun Y. (2020 c). The gut microbiota confers protection in the CNS against neurodegeneration induced by manganism. Biomed. Pharmacother., 127: 110150.
Search in Google Scholar Back to article
Wang H., Yang F., Xin R., Cui D., He J., Zhang S., Sun Y. (2020 a). The gut microbiota attenuate neuroinflammation in manganese exposure by inhibiting cerebral NLRP3 inflammasome. Biomed. Pharmacother., 129: 110449.
Search in Google Scholar Back to article
Wang M., Huang H., Hu Y., Huang J., Yang H., Wang L., Chen S., Chen C., He S. (2020 b). Effects of dietary microencapsulated tannic acid supplementation on the growth performance, intestinal morphology, and intestinal microbiota in weaning piglets. J. Anim. Sci., 98: skaa112.
Search in Google Scholar Back to article
Wang F., Yin Y., Yang M., Chen J., Fu C., Huang K. (2021). Effects of combined supplementation of Macleaya cordata extract and benzoic acid on the growth performance, immune responses, antioxidant capacity, intestinal morphology, and microbial composition in weaned piglets. Front. Vet. Sci., 8: 708597.
Search in Google Scholar Back to article
Wang X., Liu Y., Wu Z., Zhang P., Zhang X. (2022). Tea polyphenols: A natural antioxidant regulates gut flora to protect the intestinal mucosa and prevent chronic diseases. Antioxidants, 11: 253.
Search in Google Scholar Back to article
Wei Z., Zhao Y., Zhang N., Han Z., Liu X., Jiang A., Zhang Y., Wang C., Gong P., Li J., Zhang X., Yang Z. (2019). Eimeria tenella induces the release of chicken heterophil extracellular traps. Vet. Parasitol., 275: 108931.
Search in Google Scholar Back to article
Wei X., Bottoms K.A., Stein H.H., Blavi L., Bradley C.L., Bergstrom J., Knapp J., Story R., Maxwell C., Tsai T., Zhao J. (2021). Dietary organic acids modulate gut microbiota and improve growth performance of nursery pigs. Microorganisms, 9: 110.
Search in Google Scholar Back to article
Wickramasuriya S.S., Park I., Lee K., Lee Y., Kim W.H., Nam H., Lillehoj H.S. (2022). Role of physiology, immunity, microbiota, and infectious diseases in the gut health of poultry. Vaccines, 10: 172.
Search in Google Scholar Back to article
Wiertsema S.P., van Bergenhenegouwen J., Garssen J., Knippels L.M.J. (2021). The interplay between the gut microbiome and the immune system in the context of infectious diseases throughout life and the role of nutrition in optimizing treatment strategies. Nutrients, 13: 886.
Search in Google Scholar Back to article
Windisch W., Schedle K., Plitzner C., Kroismayr A. (2008). Use of phytogenic products as feed additives for swine and poultry. J. Anim. Sci., 86: E140–148.
Search in Google Scholar Back to article
Winiarska-Mieczan A. (2013). Protective effect of tannic acid on the brain of adult rats exposed to cadmium and lead. Environ. Toxicol. Pharmacol., 36: 9–18.
Search in Google Scholar Back to article
Winiarska-Mieczan A. (2018). Protective effect of tea against lead and cadmium-induced oxidative stress – a review. Biometals, 31: 909–926.
Search in Google Scholar Back to article
Winiarska-Mieczan A., Jachimowicz K., Kwiecień M., Kislova S., Baranowska-Wójcik E., Zasadna Z., Yanovych D., Kowalczuk-Vasilev E. (2021). The impact of Zn, Cu and Fe chelates on the fatty-acid profile and dietary value of broiler-chicken thigh meat. Animals, 11: 3115.
Search in Google Scholar Back to article
Wisselink H.J., Cornelissen J.B.W.J., Mevius D.J., Smits M.A., Smidt H., Rebel J.M.J. (2017). Antibiotics in 16-day-old broilers temporarily affect microbial and immune parameters in the gut. Poultry Sci., 96: 3068–3078.
Search in Google Scholar Back to article
Wu B., Cui H., Peng X., Pan K., Fang J., Zuo Z., Deng J., Wang X., Huang J. (2014). Toxicological effects of dietary nickel chloride on intestinal microbiota. Ecotoxicol. Environ. Saf., 109: 70–76.
Search in Google Scholar Back to article
Wu J., Wen X.W., Faulk C., Boehnke K., Zhang H., Dolinoy D.C., Xi C. (2016). Perinatal lead exposure alters gut microbiota composition and results in sex-specific bodyweight increases in adult mice. Toxicol. Sci., 151: 324–333.
Search in Google Scholar Back to article
Xin J., Zeng D., Wang H., Sun N., Zhao Y., Dan Y., Pan K., Jing B., Ni X. (2020). Probiotic Lactobacillus johnsonii BS15 promotes growth performance, intestinal immunity, and gut microbiota in piglets. Probiotics Antimicrob. Proteins, 12: 184–193.
Search in Google Scholar Back to article
Xiong X., Yang H.S., Wang X.C., Hu Q., Liu C.X., Wu X., Deng D., Hou Y.Q., Nyachoti C.M., Xiao D.F., Yin Y.L. (2015). Effect of low dosage of chito-oligosaccharide supplementation on intestinal morphology, immune response, antioxidant capacity, and barrier function in weaned piglets. J. Anim. Sci., 93: 1089–1097.
Search in Google Scholar Back to article
Xiong J., Qiu H., Bi Y., Zhou H., Guo S., Ding B. (2018). Effects of dietary supplementation with tributyrin and coated sodium butyrate on intestinal morphology, disaccharidase activity and intramuscular fat of lipopolysaccharide-challenged broilers. Braz. J. Poult. Sci., 20: 707–716.
Search in Google Scholar Back to article
Yang J., Xu Y., Qian K., Zhang W., Wu D., Wang C. (2016). Effects of chromium-enriched Bacillus subtilis KT260179 supplementation on growth performance, caecal microbiology, tissue chromium level, insulin receptor expression and plasma biochemical profile of mice under heat stress. Br. J. Nutr., 115: 774–781.
Search in Google Scholar Back to article
Yang J., Qian K., Wang C., Wu Y. (2018). Roles of probiotic Lactobacilli inclusion in helping piglets establish healthy intestinal inter-environment for pathogen defense. Probiotics Antimicrob. Proteins., 10: 243–250.
Search in Google Scholar Back to article
Yang Z., Wang Y., He T., Ziema Bumbie G., Wu L., Sun Z., Sun W., Tang Z. (2021 a). Effects of dietary Yucca schidigera extract and oral Candida utilis on growth performance and intestinal health of weaned piglets. Front. Nutr., 8: 685540.
Search in Google Scholar Back to article
Yang C., Diarra M.S., Choi J., Rodas-Gonzalez A., Lepp D., Liu S., Lu P., Mogire M., Gong J., Wang Q., Yang C. (2021 b). Effects of encapsulated cinnamaldehyde on growth performance, intestinal digestive and absorptive functions, meat quality and gut microbiota in broiler chickens. Transl. Anim. Sci., 5: txab099.
Search in Google Scholar Back to article
Yazdankhah S., Rudi K., Bernhoft A. (2014). Zinc and copper in animal feed – development of resistance and co-resistance to antimicrobial agents in bacteria of animal origin. Microb. Ecol. Health Dis., 25: 1–7.
Search in Google Scholar Back to article
Ye Y., Li Z., Wang P., Zhu B., Zhao M., Huang D., Ye Y., Ding Z., Li L., Wan G., Wu Q., Song D., Tang Y. (2021). Effects of probiotic supplements on growth performance and intestinal microbiota of partridge shank broiler chicks. PeerJ., 9: e12538.
Search in Google Scholar Back to article
Yu L., Yu Y., Yin R., Duan H., Qu D., Tian F., Narbad A., Chen W., Zhai Q. (2021). Dose-dependent effects of lead induced gut injuries: An in vitro and in vivo study. Chemosphere, 266: 129130.
Search in Google Scholar Back to article
Yuan Z.H., Wang J.P., Zhang K.Y., Ding X.M., Bai S.P., Zeng Q.F., Xuan Y., Su Z.W. (2016). Effect of vanadium and tea polyphenols on intestinal morphology, microflora and Short-Chain fatty acid profile of laying hens. Biol. Trace Elem. Res., 174: 419–427.
Search in Google Scholar Back to article
Zandi P., Schnug E. (2022). Reactive oxygen species, antioxidant responses and implications from a microbial modulation perspective. Biology, 11: 155.
Search in Google Scholar Back to article
Zhai Q., Tian F., Zhao J., Zhang H., Narbad A., Chen W. (2016). Oral administration of probiotics inhibits absorption of the heavy metal cadmium by protecting the intestinal barrier. Appl. Environ. Microbiol., 82: 4429–4440.
Search in Google Scholar Back to article
Zhai Q., Qu D., Feng S., Yu Y., Yu L., Tian F., Zhao J., Zhang H., Chen W. (2020). Oral supplementation of lead-intolerant intestinal microbes protects against lead (Pb) toxicity in mice. Front. Microbiol., 10: 3161.
Search in Google Scholar Back to article
Zhang Y., Wang Y., Chen D., Yu B., Zheng P., Mao X., Luo Y., Li Y., He J. (2018). Dietary chlorogenic acid supplementation affects gut morphology, antioxidant capacity and intestinal selected bacterial populations in weaned piglets. Food Funct., 9: 4968–4978.
Search in Google Scholar Back to article
Zhang B.B., Liu Y.M., Hu A.L., Xu S.F., Fan L.D., Cheng M.L., Li C., Wei L.X., Liu J. (2019). HgS and Zuotai differ from HgCl2 and methyl mercury in intestinal Hg absorption, transporter expression and gut microbiome in mice. Toxicol. Appl. Pharmacol., 379: 114615.
Search in Google Scholar Back to article
Zhang Z., Cao H., Song N., Zhang L., Cao Y., Tai J. (2020). Longterm hexavalent chromium exposure facilitates colorectal cancer in mice associated with changes in gut microbiota composition. Food Chem. Toxicol., 138: 111237.
Search in Google Scholar Back to article
Zhao Y., Zhou C., Wu C., Guo X., Hu G., Wu Q., Xu Z., Li G., Cao H., Li L., Latigo V., Liu P., Cheng S., Liu P. (2020). Subchronic oral mercury caused intestinal injury and changed gut microbiota in mice. Sci. Total. Environ., 721: 137639.
Search in Google Scholar Back to article
Zhao Y., Zhang H., Hao D., Wang J., Zhang D., Sun Z., Liu C. (2022). Selenium alleviates chromium(VI)-induced ileum damage and cecal microbial disturbances in mice. Biol. Trace Elem. Res., doi: 10.1007/s12011-021-03061-x. (online ahead of print).
Search in Google Scholar Back to article
Zhou S., Wei C., Liao C., Wu H. (2008). Damage to DNA of effective microorganisms by heavy metals: Impact on wastewater treatment. J. Environ. Sci. (China), 20: 1514–1518.
Search in Google Scholar Back to article
Zhou X., Li J., Sun J.L. (2019). Oral nickel changes of intestinal microflora in mice. Curr. Microbiol., 76: 590–596.
Search in Google Scholar Back to article
Zhou C., Xu P., Huang C., Liu G., Chen S., Hu G., Li G., Liu P., Guo X. (2020). Effects of subchronic exposure of mercuric chloride on intestinal histology and microbiota in the cecum of chicken. Ecotoxicol. Environ. Saf., 188: 109920.
Search in Google Scholar Back to article

Bioactive compounds, antibiotics and heavy metals: Effects on the intestinal structure and microbiome of monogastric animals – a non-systematic review

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