No protective effects of high-dosage dietary zinc oxide on weaned pigs infected with Salmonella enterica serovar typhimurium DT104

Applied and Environmental Microbiology

Volumn 79, Issue 9, 2013, Pages 2914-2921

  Janczyk, Pawel ^a   Kreuzer, Susanne ^b   Assmus, Jens ^b   Nöckler, Karsten ^a   Brockmann, Gudrun A ^b  

^a FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIETARY ZINC OXIDE; GROWTH PERFORMANCE; GUT-ASSOCIATED LYMPHATIC TISSUES; IMMUNE RESPONSE; PROTECTIVE EFFECTS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM; ZINC OXIDE (ZNO);

BLOOD; CELLS; CYTOLOGY; IMMUNE SYSTEM; NUTRITION; SALMONELLA; TISSUE; ZINC; ZINC OXIDE;

MAMMALS;

ARTIFICIAL DIET; BACTERIAL DISEASE; BLOOD; CONCENTRATION (COMPOSITION); FECES; FOOD SUPPLEMENTATION; GROWTH RATE; IMMUNE RESPONSE; IMMUNE SYSTEM; LIVESTOCK FARMING; MUCUS; PIG; WEANING; ZINC;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM; SUIDAE;

BACTERIUM ANTIBODY; IMMUNOGLOBULIN G; ZINC OXIDE;

ADAPTIVE IMMUNITY; ANIMAL; ANIMAL FOOD; B LYMPHOCYTE; BACTERIAL SHEDDING; DIET SUPPLEMENTATION; DOSE RESPONSE; DRUG EFFECTS; FECES; FEMALE; GROWTH, DEVELOPMENT AND AGING; HUMORAL IMMUNITY; IMMUNOLOGY; MALE; MICROBIOLOGY; RANDOMIZATION; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA INFECTIONS, ANIMAL; SWINE; SWINE DISEASES; T LYMPHOCYTE; TIME; WEANING;

ADAPTIVE IMMUNITY; ANIMAL FEED; ANIMALS; ANTIBODIES, BACTERIAL; B-LYMPHOCYTES; BACTERIAL SHEDDING; DIETARY SUPPLEMENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; FECES; FEMALE; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; MALE; RANDOM ALLOCATION; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SWINE; SWINE DISEASES; T-LYMPHOCYTES; TIME FACTORS; WEANING; ZINC OXIDE;

EID: 84876302106     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03577-12     Document Type: Article

References (42)

1. Chasapis CT, Loutsidou AC, Spiliopoulou CA, Stefanidou ME. 2012. Zinc and human health: an update. Arch. Toxicol. 86:521-534.
2. Fraker PJ, King LE, Laakko T, Vollmer TL. 2000. The dynamic link between the integrity of the immune system and zinc status. J. Nutr. 130: 1399S-1406S.
3. Gupta DN, Mondal SK, Ghosh S, Rajendran K, Sur D, Manna B. 2003. Impact of zinc supplementation on diarrhoeal morbidity in rural children of West Bengal, India. Acta Paediatr. 92:531-536.
4. Rahman MM, Vermund SH, Wahed MA, Fuchs GJ, Baqui AH, Alvarez JO. 2001. Simultaneous zinc and vitamin A supplementation in Bangladeshi children: randomised double blind controlled trial. BMJ 323:314-318.
5. National Research Council. 1998. Nutrient requirements of swine, 10th rev ed, p 56. National Academy Press, Washington, DC.
6. Gesellschaft für Ernährungsphysiologie der Haustiere. Ausschuss für Bedarfsnormen. 2006. Energie- und Nährstoffbedarf landwirtschaftlicher Nutztiere, vol 4. Empfehlungen zur Energie- und Nährstoffversorgung der Schweine, 10th ed. DLG-Verlag, Frankfurt am Main, Germany.
7. Poulsen HD. 1995. Zinc oxide for weanling piglets. Acta Agric. Scand. Sect. A 45:159 -167.
8. Richards JD, Zhao J, Harrell RJ, Atwell CA, Dibner JJ. 2010. Trace mineral nutrition in poultry and swine. Asian-Aust. J. Anim. Sci. 23:1527-1534.
9. European Community. 26 July 2003. Commission Regulation (EC) no. 1334/2003 of 25 July 2003 amending the conditions for authorisation of a number of additives in feedingstuffs belonging to the group of trace elements. Off. J. Eur. Union L 187:11-15. http://eur-lex.europa.eu/LexUri Serv/LexUriServ.do?uri=CELEX:32003R1334:EN:HTML.
10. Molist F, Hermes RG, de Segura AG, Martin-Orue SM, Gasa J, Manzanilla EG, Perez JF. 2011. Effect and interaction between wheat bran and zinc oxide on productive performance and intestinal health in postweaning piglets. Br. J. Nutr. 105:1592-1600.
11. Shelton NW, Tokach MD, Nelssen JL, Goodband RD, Dritz SS, Derouchey JM, Hill GM. 2011. Effects of copper sulfate, tri-basic copper chloride, and zinc oxide on weanling pig performance. J. Anim. Sci. 89: 2440-2451.
12. Højberg O, Canibe J, Poulsen HD, Hedemann MS, Jensen BB. 2005. Influence of dietary zinc oxide and copper sulfate on the intestinal ecosystem in newly weaned piglets. Appl. Environ. Microbiol. 71:2267-2277.
13. Vahjen W, Pieper R, Zentek J. 2011. Increased dietary zinc oxide changes the bacterial core and enterobacterial composition in the ileum of piglets. J. Anim. Sci. 89:2430-2439.
14. Pieper R, Vahjen W, Neumann K, Van Kessel AG, 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. (Berl.) 96:825-833.
15. Kaiser P, Hardt WD. 2011. Salmonella Typhimurium diarrhea: switching the mucosal epithelium from homeostasis to defense. Curr. Opin. Immunol. 23:456-463.
16. Hallstrom K, McCormick BA. 2011. Salmonella interaction with and passage through the intestinal mucosa: through the lens of the organism. Front. Microbiol. 2:88. doi:10.3389/fmicb.2011.00088.
17. Szabó I, Wieler LH, Tedin K, Scharek-Tedin L, Taras D, Hensel A, Appe B, Noeckler K. 2009. Influence of a probiotic strain of Enterococcus faecium on Salmonella enterica serovar Typhimurium DT104 infection in a porcine animal infection model. Appl. Environ. Microbiol. 75:2621-2628.
18. Kreuzer S, Janczyk P, Assmus J, Schmidt MF, Brockmann GA, Nockler K. 2012. No beneficial effects evident for Enterococcus faecium NCIMB 10415 in weaned pigs infected with Salmonella enterica serovar Typhimurium DT104. Appl. Environ. Microbiol. 78:4816-4825.
19. European Food Safety Authority. 2010. The Community Summary Report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J. 8(1):1496. doi:10.2903/j.efsa.2010.1496.
20. Fravalo P, Hascoet Y, le Fellic M, Queguiner S, Petton J, Salvat G. 2003. Convenient method for rapid and quantitative assessment of Salmonella enterica contamination: the mini-MSRV MPN technique. J. Rapid Methods Automat. Microbiol. 11:81- 88.
21. Malorny B, Paccassoni E, Fach P, Bunge C, Martin A, Helmuth R. 2004. Diagnostic real-time PCR for detection of Salmonella in food. Appl. Environ. Microbiol. 70:7046-7052.
22. Kreuzer S, Machnowska P, Assmus J, Sieber M, Pieper R, Schmidt MF, Brockmann GA, Scharek-Tedin L, Johne R. 2012. Feeding of the probiotic bacterium Enterococcus faecium NCIMB 10415 differentially affects shedding of enteric viruses in pigs. Vet. Res. 43:58. doi:10.1186/1297-9716-43-58.
23. Van Boxstael S, Dierick K, Van Huffel X, Uyttendaele M, Berkvens D, Herman L, Bertrand S, Wildemauwe C, Catry B, Butaye P, Imberechts H. 2012. Comparison of antimicrobial resistance patterns and phage types of Salmonella Typhimurium isolated from pigs, pork and humans in Belgium between 2001 and 2006. Food Res. Int. 45:913-918.
24. Sinkora M, Butler JE. 2009. The ontogeny of the porcine immune system. Dev. Comp. Immunol. 33:273-283.
25. Carlson MS, Hill GM, Link JE. 1999. Early- and traditionally weaned nursery pigs benefit from phase-feeding pharmacological concentrations of zinc oxide: effect on metallothionein and mineral concentrations. J. Anim. Sci. 77:1199-1207.
26. Hollis GR, Carter SD, Cline TR, Crenshaw TD, Cromwell GL, Hill GM, Kim SW, Lewis AJ, Mahan DC, Miller PS, Stein HH, Veum TL. 2005. Effects of replacing pharmacological levels of dietary zinc oxide with lower dietary levels of various organic zinc sources for weanling piglets. J. Anim. Sci. 83:2123-2129.
27. Wang Y, Tang JW, Ma WQ, Feng J, Feng J. 26 June 2009. Dietary zinc glycine chelate on growth performance, tissue mineral concentrations, and serum enzyme activity in weanling piglets. Biol. Trace Elem. Res. {left open bracket}Epub ahead of print.{right open bracket} doi:10.1007/s12011-009-8437-3.
28. Janczyk P, Pieper R, Smidt H, Souffrant WB. 2010. Effect of alginate and inulin on intestinal microbial ecology of weanling pigs reared under different husbandry conditions. FEMS Microbiol. Ecol. 72:132-142.
29. Surjawidjaja JE, Hidayat A, Lesmana M. 2004. Growth inhibition of enteric pathogens by zinc sulfate: an in vitro study. Med. Princ. Pract. 13:286-289.
30. Jensen-Waern M, Melin L, Lindberg R, Johannisson A, Petersson L, Wallgren P. 1998. Dietary zinc oxide in weaned pigs-effects on performance, tissue concentrations, morphology, neutrophil functions and faecal microflora. Res. Vet. Sci. 64:225-231.
31. Bratz K, Gölz G, Alter T, Bücker R, Janczyk P, Nöckler K. 2012. Effects of dietary zinc oxide and Enterococcus faecium NCIMB 10415 supplementation on Campylobacter coli levels in weaned piglets. Int. J. Med. Microbiol. 302:56. (Abstract.)
32. Mosquito S, Ruiz J, Pons MJ, Durand D, Barletta F, Ochoa TJ. 2012. Molecular mechanisms of antibiotic resistance in diarrhoeagenic Escherichia coli isolated from children, Int. J. Antimicrob. Agents 40:544-548.
33. Hsu S-C, Chiu T-H, Pang J-C, Hsuan-Yuan C-H, Chang G-N, Tsen H-Y. 2006. Characterisation of antimicrobial resistance patterns and class 1 integrons among Escherichia coli and Salmonella enterica serovar Choleraesuis strains isolated from humans and swine in Taiwan. Int. J. Antimicrob. Agents 27:383-391.
34. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, Roth JR, Bäumler AJ. 2010. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426-429.
35. Stecher B, Denzler R, Maier L, Bernet F, Sanders MJ, Pickard DJ, Barthel M, Westendorf AM, Krogfelt KA, Walker AW, Ackermann M, Dobrindt U, Thomson NR, Hardt WD. 2012. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc. Natl. Acad. Sci. U. S. A. 109:1269 -1274.
36. Ruiz J, Castro D, Goni P, Santamaria JA, Borrego JJ, Vila J. 1997. Analysis of the mechanism of quinolone resistance in nalidixic acidresistant clinical isolates of Salmonella serotype Typhimurium. J. Med. Microbiol. 46:623-628.
37. Boyd DA, Peters GA, Ng L, Mulvey MR. 2000. Partial characterization of a genomic island associated with the multidrug resistance region of Salmonella enterica Typhimurium DT104. FEMS Microbiol. Lett. 189:285-291.
38. Vo ATT, van Duijkeren A, Gaastra W, Fluit AC. 2010. Antimicrobial resistance, class 1 integrons, and genomic island 1 in Salmonella isolates from Vietnam. PLoS One 5:e9440. doi:10.1371/journal.pone.0009440.
39. Doublet B, Boyd D, Mulvey MR, Cloeckaert A. 2005. The Salmonella genomic island 1 is an integrative mobilizable element. Mol. Microbiol. 55:1911-1924.
40. Misselwitz B, Barrett N, Kreibich S, Vonaesch P, Andritschke D, Rout S, Weidner K, Sormaz M, Songhet P, Horvath P, Chabria M, Vogel V, Spori DM, Jenny P, Hardt WD. 2012. Near surface swimming of Salmonella Typhimurium explains target-site selection and cooperative invasion. PLoS Pathog. 8:e1002810. doi:10.1371/journal.ppat.1002810.
41. Van Parys A, Boyen F, Verbrugghe E, Leyman B, Bram F, Haesebrouck F, Pasmans F. 2012. Salmonella Typhimurium induces SPI-1 and SPI-2 regulated and strain dependent downregulation of MHC II expression on porcine alveolar macrophages. Vet. Res. 43:52. doi:10.1186/1297-9716-43-52.
42. Müller AJ, Kaiser P, Dittmar KE, Weber TC, Haueter S, Endt K, Songhet P, Zellweger C, Kremer M, Fehling HJ, Hardt WD. 2012. Salmonella gut invasion involves TTSS-2-dependent epithelial traversal, basolateral exit, and uptake by epithelium-sampling lamina propria phagocytes. Cell Host Microbe 11:19 -32.