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Effect of zinc on growth performance, gut morphometry, and cecal microbial community in broilers challenged with Salmonella enterica serovar typhimurium

  • Microbial Ecology and Environmental Microbiology
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Abstract

To evaluate the effects of supplemental zinc on growth performance, gut morphometry, and the cecal microbial community in broilers challenged with Salmonella typhimurium, 180, 1-day-old male Cobb 500 broiler chicks were randomly assigned to 3 treatments with ten replicates for a 42 day experiment. The 3 treatments were: unchallenged, S. typhimurium-challenged, and S. typhimurium-challenged with 120 mg/kg of zinc supplementation in the diet. Salmonella infection caused a reduction in body-weight gain and feed intake, disrupted the intestinal structure by decreasing the villus-height/crypt-depth ratio of the ileum and increasing the apoptotic index of ileal epithelial cells. Moreover, the cecal microbial community was altered by Salmonella infection, as demonstrated by a reduced number of Lactobacillus and total bacteria. Dietary zinc supplementation improved growth performance by increasing the body-weight gain and feed intake in the challenged broilers. In addition, zinc repaired intestinal injury by reducing the apoptotic index of ileal epithelial cells, enhancing villus height and the villus-height/crypt-depth ratio of the ileum, and the proliferation index of ileal epithelial cells. Finally, zinc regulated the cecal microbial community by increasing the number of total bacteria and beneficial Lactobacillus bacteria, and reducing the number of Salmonella. The results indicated that dietary zinc supplementation improved growth performance, intestinal morphology, and intestinal microbiota in S. typhimurium-challenged broilers.

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References

  • Amit-Romach, E., Sklan, D., and Uni, Z. 2004. Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult. Sci. 83, 1093–1098.

    Article  CAS  PubMed  Google Scholar 

  • Barman, M., Unold, D., Shifley, K., Amir, E., Hung, K., Bos, N., and Salzman, N. 2008. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect. Immun. 76, 907–915.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barnes, E.M., Impey, C.S., and Cooper, D.M. 1980. Manipulation of the crop and intestinal flora of the newly hatched chick. Am. J. Clin. Nutr. 33, 2426–2433.

    CAS  PubMed  Google Scholar 

  • Barrow, P.A., Huggins, M.B., Lovell, M.A., and Simpson, J.M. 1987. Observations on the pathogenesis of experimental Salmonella typhimurium infection in chickens. Res. Vet. Sci. 42, 194–199.

    CAS  PubMed  Google Scholar 

  • Barrow, P.A., Simpson, J.M., and Lovell, M.A. 1988. Intestinal colonisation in the chicken by food-poisoning Salmonella serotypes; Microbial characteristics associated with faecal excretion. Avian Pathol. 17, 571–588.

    Article  CAS  PubMed  Google Scholar 

  • Bartosch, S., Fite, A., Macfarlane, T., and McMurdo, M.E. 2004. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using realtime PCR and effects of antibiotic treatment on the fecal microbiota. Appl. Environ. Microbiol. 70, 3575–3581.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ben, O.N. and Ampe, F. 2000. Microbial community dynamics during production of the Mexican fermented maize dough pozol. Appl. Environ. Microbiol. 66, 3664–3673.

    Article  Google Scholar 

  • Berndt, A., Wilhelm, A., Jugert, C., Pieper, J., Sachse, K., and Methner, U. 2007. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect. Immun. 75, 5993–6007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brandão-Neto, J., Stefan, V., Mendonça, B.B., Bloise, W., and Castro, A.V.B. 1995. The essential role of zinc in growth. Nutr. Res. 15, 335–358.

    Article  Google Scholar 

  • Cario, E., Jung, S., Harder, D.J., Schulte, C., Sturm, A., Wiedenmann, B., Goebell, H., and Dignass, A.U. 2000. Effects of exogenous zinc supplementation on intestinal epithelial repair in vitro. Eur. J. Clin. Invest. 30, 419–428.

    Article  CAS  PubMed  Google Scholar 

  • Chambers, J.R. and Gong, J. 2011. The intestinal microbiota and its modulation for Salmonella control in chickens. Food Res. Int. 44, 3149–3159.

    Article  Google Scholar 

  • Fang, H. 2010. Inhibitory effects of Lactobacillus casei subsp. rhamnosus on Salmonella lipopolysaccharideinduced inflammation and epithelial barrier. J. Med. Microbiol. 59, 573–579.

    Article  CAS  PubMed  Google Scholar 

  • Fasina, Y.O., Hoerr, F.J., McKee, S.R., and Conner, D.E. 2010. Influence of Salmonella enterica serovar Typhimurium infection on intestinal goblet cells and villous morphology in broiler chicks. Avian Dis. 54, 841–847.

    Article  CAS  PubMed  Google Scholar 

  • Foley, J., Ton, T., Maronpot, R., Butterworth, B., and Goldsworthy, T.L. 1993. Comparison of proliferating cell nuclear antigen to tritiated thymidine as a marker of proliferating hepatocytes in rats. Environ. Health Perspect. 101 (Suppl 5), 199–205.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo, X., Xia, X., Tang, R., Zhou, J., Zhao, H., and Wang, K. 2008. Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett. Appl. Microbiol. 47, 367–373.

    Article  CAS  PubMed  Google Scholar 

  • Hadjinicolaou, A.V., Demetriou, V.L., Emmanuel, M.A., Kakoyiannis, C.K., and Kostrikis, L.G. 2009. Molecular beacon-based real-time PCR detection of primary isolates of Salmonella Typhimurium and Salmonella Enteritidis in environmental and clinical samples. BMC Microbiol. 9, 97.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hegazy, S.M. and Adachi, Y. 2000. Comparison of the effects of dietary selenium, zinc, and selenium and zinc supplementation on growth and immune response between chick groups that were inoculated with Salmonella and aflatoxin or Salmonella. Poult. Sci. 79, 331–335.

    Article  CAS  PubMed  Google Scholar 

  • Hojberg, O., Canibe, N., Poulsen, H.D., Hedemann, M.S., and Jensen, B.B. 2005. Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned piglets. Appl. Environ. Microbiol. 71, 2267–2277.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu, C., Song, J., Li, Y., Luan, Z., and Zhu, K. 2013. Diosmectite-zinc oxide composite improves intestinal barrier function, modulates expression of pro-inflammatory cytokines and tight junction protein in early weaned pigs. Br. J. Nutr. 110, 681–688.

    Article  CAS  PubMed  Google Scholar 

  • Johansen, C.H., Bjerrum, L., and Pedersen, K. 2007. Impact of salinomycin on the intestinal microflora of broiler chickens. Acta Vet. Scand. 49, 30.

    Article  PubMed Central  PubMed  Google Scholar 

  • Jones, S.E. and Versalovic, J. 2009. Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol. 9, 35.

    Article  PubMed Central  PubMed  Google Scholar 

  • Juricova, H., Videnska, P., Lukac, M., Faldynova, M., Babak, V., Havlickova, H., Sisak, F., and Rychlik, I. 2013. Influence of Salmonella enterica serovar enteritidis infection on the development of the cecum microbiota in newly hatched chicks. Appl. Environ. Microbiol. 79, 745–747.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim, J.M., Eckmann, L., Savidge, T.C., Lowe, D.C., Witthöft, T., and Kagnoff, M.F. 1998. Apoptosis of human intestinal epithelial cells after bacterial invasion. J. Clin. Invest. 102, 1815.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lamb-Rosteski, J.M., Kalischuk, L.D., Inglis, G.D., and Buret, A.G. 2008. Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation. Infect. Immun. 76, 3390–3398.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lan, Y., Verstegen, M., Tamminga, S., and Williams, B.A. 2005. The role of the commensal gut microbial community in broiler chickens. World’s Poultry Sci. J. 61, 95–104.

    Article  Google Scholar 

  • Ley, R.E., Turnbaugh, P.J., Klein, S., and Gordon, J.I. 2006. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023.

    Article  CAS  PubMed  Google Scholar 

  • Lim, Y.H., Hirose, K., Izumiya, H., Arakawa, E., Takahashi, H., Terajima, J., Itoh, K., Tamura, K., Kim, S.I., and Watanabe, H. 2003. Multiplex polymerase chain reaction assay for selective detection of Salmonella enterica serovar Typhimurium. Jpn. J. Infect. Dis. 56, 151–155.

    CAS  PubMed  Google Scholar 

  • Liu, J.Z., Jellbauer, S., Poe, A.J., Ton, V., Pesciaroli, M., Kehl-Fie, T.E., Restrepo, N.A., Hosking, M.P., Edwards, R.A., Battistoni, A., and et al. 2012. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell. Host. Microbe 11, 227–239.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lynch, M.J., Leon-Velarde, C.G., McEwen, S., and Odumeru, J.A. 2004. Evaluation of an automated immunomagnetic separation method for the rapid detection of Salmonella species in poultry environmental samples. J. Microbiol. Methods 58, 285–288.

    Article  CAS  PubMed  Google Scholar 

  • MacDonald, R.S. 2000. The role of zinc in growth and cell proliferation. J. Nutr. 130, 1500S–1508S.

    CAS  PubMed  Google Scholar 

  • Marcq, C., Cox, E., Szalo, I.M., Thewis, A., and Beckers, Y. 2011. Salmonella Typhimurium oral challenge model in mature broilers: Bacteriological, immunological, and growth performance aspects. Poult. Sci. 90, 59–67.

    Article  CAS  PubMed  Google Scholar 

  • McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., Porwollik, S., Ali, J., Dante, M., Du, F., and et al. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413, 852–856.

    Article  CAS  PubMed  Google Scholar 

  • Mocchegiani, E., Costarelli, L., Basso, A., Giacconi, R., Piacenza, F., and Malavolta, M. 2013. Metallothioneins, ageing and cellular senescence: A future therapeutic target. Curr. Pharm. Design 19, 1753–1764.

    CAS  Google Scholar 

  • Paesold, G., Guiney, D.G., Eckmann, L., and Kagnoff, M.F. 2002. Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells. Cell Microbiol. 4, 771–781.

    Article  CAS  PubMed  Google Scholar 

  • Pezoa, D., Yang, H.J., Blondel, C.J., Santiviago, C.A., Andrews-Polymenis, H.L., and Contreras, I. 2013. The type VI secretion system encoded in SPI-6 plays a role in gastrointestinal colonization and systemic spread of Salmonella enterica serovar Typhimurium in the chicken. PLoS One 8, e63917.

    Article  Google Scholar 

  • Powell, S. R. 2000. The antioxidant properties of zinc. J. Nutr. 130, 1447S–1454S.

    CAS  PubMed  Google Scholar 

  • Revolledo, L., Ferreira, C.S., and Ferreira, A.J. 2009. Prevention of Salmonella Typhimurium colonization and organ invasion by combination treatment in broiler chicks. Poult. Sci. 88, 734–743.

    Article  CAS  PubMed  Google Scholar 

  • Ricca, D.M., Ziemer, C.J., and Kerr, B.J. 2010. Changes in bacterial communities from swine feces during continuous culture with starch. Anaerobe 16, 516–521.

    Article  CAS  PubMed  Google Scholar 

  • Rinttila, T., Kassinen, A., Malinen, E., Krogius, L., and Palva, A. 2004. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J. Appl. Microbiol. 97, 1166–1177.

    Article  CAS  PubMed  Google Scholar 

  • Roselli, M., Finamore, A., Garaguso, I., Britti, M.S., and Mengheri, E. 2003. Zinc oxide protects cultured enterocytes from the damage induced by Escherichia coli. J. Nutr. 133, 4078–4082.

    Google Scholar 

  • Shao, Y., Guo, Y., and Wang, Z. 2013. Beta-1,3/1,6-glucan alleviated intestinal mucosal barrier impairment of broiler chickens challenged with Salmonella enterica serovar Typhimurium. Poult. Sci. 92, 1764–1773.

    Article  CAS  PubMed  Google Scholar 

  • Simpson, E.H. 1949. Measurement of diversity. Nature 163, 688.

    Article  Google Scholar 

  • Smith, J.C., McDaniel, E.G., McBean, L.D., Doft, F.S., and Halsted, J.A. 1972. Effect of microorganisms upon zinc metabolism using germfree and conventional rats. J. Nutr. 102, 711–719.

    CAS  PubMed  Google Scholar 

  • Sokol, H., Seksik, P., Rigottier Gois, L., Lay, C., Lepage, P., Podglajen, I., Marteau, P., and Doré, J. 2006. Specificities of the fecal microbiota in inflammatory bowel disease. Inflamm. Bowel Dis. 12, 106–111.

    Article  PubMed  Google Scholar 

  • Sommer, F. and Backhed, F. 2013. The gut microbiota—masters of host development and physiology. Nat. Rev. Microbiol. 11, 227–238.

    Article  CAS  PubMed  Google Scholar 

  • Southon, S., Gee, J.M., Bayliss, C.E., Wyatt, G.M., Horn, N., and Johnson, I.T. 1986. Intestinal microflora, morphology and enzyme activity in zinc-deficient and Zn-supplemented rats. Br. J. Nutr. 55, 603–611.

    Article  CAS  PubMed  Google Scholar 

  • Starke, I.C., Pieper, R., Neumann, K., Zentek, J., and Vahjen, W. 2013. The impact of high dietary zinc oxide on the development of the intestinal microbiota in weaned piglets. FEMS Microbiol. Ecol. 87, 416–427.

    Article  PubMed  Google Scholar 

  • Stecher, B., Robbiani, R., Walker, A.W., Westendorf, A.M., Barthel, M., Kremer, M., Chaffron, S., Macpherson, A.J., Buer, J., Parkhill, J., and et al. 2007. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5, 2177–2189.

    Article  CAS  PubMed  Google Scholar 

  • Summers, R.J. and Srinivasan, V.R. 1979. Macromolecular composition of a Cellulomonas sp. Cultivated in continuous culture under glucose and zinc limitation. Appl. Environ. Microbiol. 37, 1079–1084.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamboli, C.P., Neut, C., Desreumaux, P., and Colombel, J.F. 2004. Dysbiosis in inflammatory bowel disease. Gut 53, 1–4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Truong-Tran, A.Q., Carter, J., Ruffin, R.E., and Zalewski, P.D. 2001. The role of zinc in caspase activation and apoptotic cell death. Biometals 14, 315–330.

    Article  CAS  PubMed  Google Scholar 

  • Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrin, V., Mardis, E.R., and Gordon, J.I. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031.

    Article  PubMed  Google Scholar 

  • Vallee, B.L., Falchuk, K.H., and Chesters, J.K. 1981. Zinc and gene expression [and discussion]. Philos. T. Roy. Soc. B. 294, 185–197.

    Article  CAS  Google Scholar 

  • Vandeplas, S., Dauphin, R.D., Thiry, C., Beckers, Y., Welling, G.W., Thonart, P., and Thewis, A. 2009. Efficiency of a Lactobacillus plantarum-xylanase combination on growth performances, microflora populations, and nutrient digestibilities of broilers infected with Salmonella Typhimurium. Poult. Sci. 88, 1643–1654.

    Article  CAS  PubMed  Google Scholar 

  • Vetuschi, A., Latella, G., Sferra, R., Caprilli, R., and Gaudio, E. 2002. Increased proliferation and apoptosis of colonic epithelial cells in dextran sulfate sodium-induced colitis in rats. Digest. Dis. Sci. 47, 1447–1457.

    Article  PubMed  Google Scholar 

  • Videnska, P., Sisak, F., Havlickova, H., Faldynova, M., and Rychlik, I. 2013. Influence of Salmonella enterica serovar Enteritidis infection on the composition of chicken cecal microbiota. BMC. Vet. Res. 9, 140.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wallis, T.S. and Galyov, E.E. 2000. Molecular basis of Salmonella-induced enteritis. Mol. Microbiol. 36, 997–1005.

    Article  CAS  PubMed  Google Scholar 

  • Walter, J., Tannock, G.W., Tilsala-Timisjarvi, A., Rodtong, S., Loach, D.M., Munro, K., and Alatossava, T. 2000. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species-specific PCR primers. Appl. Environ. Microbiol. 66, 297–303.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Walter, J., Hertel, C., Tannock, G.W., Lis, C.M., Munro, K., and Hammes, W.P. 2001. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 67, 2578–2585.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang, L.C., Zhang, T.T., Wen, C., Jiang, Z.Y., Wang, T., and Zhou, Y.M. 2012. Protective effects of zinc-bearing clinoptilolite on broilers challenged with Salmonella pullorum. Poult. Sci. 91, 1838–1845.

    Article  CAS  PubMed  Google Scholar 

  • Watson, A.J., Chu, S., Sieck, L., Gerasimenko, O., Bullen, T., Campbell, F., McKenna, M., Rose, T., and Montrose, M.H. 2005. Epithelial barrier function in vivo is sustained despite gaps in epithelial layers. Gastroenterology 129, 902–912.

    Article  PubMed  Google Scholar 

  • Wise, M.G. and Siragusa, G.R. 2007. Quantitative analysis of the intestinal bacterial community in one- to three-week-old commercially reared broiler chickens fed conventional or antibioticfree vegetable-based diets. J. Appl. Microbiol. 102, 1138–1149.

    CAS  PubMed  Google Scholar 

  • Yan, F., Cao, H., Cover, T.L., Whitehead, R., Washington, M.K., and Polk, D.B. 2007. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132, 562–575.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, B., Shao, Y., Liu, D., Yin, P., Guo, Y., and Yuan, J. 2012. Zinc prevents Salmonella enterica serovar Typhimurium-induced loss of intestinal mucosal barrier function in broiler chickens. Avian Pathol. 41, 361–367.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, H., Gong, J., Brisbin, J.T., Yu, H., Sanei, B., Sabour, P., and Sharif, S. 2007. Appropriate chicken sample size for identifying the composition of broiler intestinal microbiota affected by dietary antibiotics, using the polymerase chain reaction-denaturing gradient gel electrophoresis technique. Poult. Sci. 86, 2541–2549.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, X.Y., Zhong, T., Pandya, Y., and Joerger, R.D. 2002. 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl. Environ. Microbiol. 68, 124–137.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Shao, Y., Lei, Z., Yuan, J. et al. Effect of zinc on growth performance, gut morphometry, and cecal microbial community in broilers challenged with Salmonella enterica serovar typhimurium. J Microbiol. 52, 1002–1011 (2014). https://doi.org/10.1007/s12275-014-4347-y

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