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Protective Effects of Zinc on Salmonella Invasion, Intestinal Morphology and Immune Response of Young Pigeons Infected with Salmonella enterica Serovar Typhimurium

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Abstract

The study aimed to determine the effects of orally supplemental zinc on body weight, Salmonella invasion, serum IgA, intestinal histomorphology, and immune response of Salmonella enterica serovar Typhimurium (S. typhimurium)–challenged young pigeons. A total of 72 healthy White King pigeons (25 days old) with similar weight were randomly assigned to 3 treatments with six replicate cages. The 3 treatments were unchallenged, S. typhimurium–challenged, and S. typhimurium–challenged orally supplemented with 1 mg zinc per bird. Salmonella infection decreased (P < 0.05) the body weight, the bursa index, the serum IgA content, and the villus height/crypt depth ratio in the ileum, but increased the neutrophil proportion (P < 0.001) and the mRNA expressions of IL-1β and IL-8 in the jejunum (P < 0.05). Orally supplemental zinc reduced (P = 0.007) the bacterial load in the liver and improved (P < 0.05) the body weight, the bursa index, the serum IgA content, the villus height/crypt depth ratio, and the NOD-like receptor family pyrin domain containing 3 (NLRP3) protein expression, as well as tended to increase (P = 0.064) the protein abundance of caspase-1 of the jejunum, but did not alleviate the high level of neutrophil proportion and IL-1β mRNA expression of the jejunum (P > 0.05). The results indicated that oral zinc supplementation improved the intestinal mucosal morphology and enhanced the immune response, as well as activated caspase-1-dependent cell pyroptosis pathways in the jejunal epithelium, thereby restricting Salmonella invasion of the challenged young pigeons.

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Data availability

The data of this study will be made available on reasonable request.

The study was carried out in accordance with the guidelines set by the Animal Care and Use Committee (permit number: SYXK-2017–0005) of the Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences (IAHVM-BAAFS), Beijing, China. The protocols were approved by the Animal Care and Use Committee of IAHVM-BAAFS.

References

  1. Soncini G, Valnegri VL, Vercellotti L, Colombo F, Valle D, Franzoni M, Bersanii C (2006) Investigation of Campylobacter in reared game birds. J Food Prot 69:3021–3024

    Article  CAS  PubMed  Google Scholar 

  2. McCrea BA, Tonooka KH, VanWorth C, Boggs CL, Atwill ER (2006) Prevalence of Campylobacter and Salmonella species on farm, after transport, and at processing in specialty market poultry. Poult Sci 85:136–143

    Article  CAS  PubMed  Google Scholar 

  3. Matsubara R, Fukuda Y, Murakoshi F, Nomura O, Suzuki T, Tada C, Nakai Y (2017) Detection and molecular status of Isospora sp. from the domestic pigeon (Columba livia domestica). Parasitol Int 66:588–592

    Article  CAS  PubMed  Google Scholar 

  4. Akbarmehr J (2010) Isolation of Salmonella spp from poultry (ostrich pigeon and chicken) and detection of their hilA gene by PCR method. African Journal of Microbiology Research 4(24):2678–2681

    CAS  Google Scholar 

  5. Gong J, Zhang J, Xu M, Zhu C, Yu Y, Liu X, Kelly P, Xu B, Wand C (2014) Prevalence and fimbrial genotype distribution of poultry Salmonella isolates in China (2006 to 2012). Appl Environ Microbiol 80(2):687–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lynch MJ, Leon-Velarde CG, McEwen S, Odumeru JA (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 

  7. Pezoa D, Yang HJ, Blondel CJ, Santiviago CA, Andrews-Polymenis HL, Contreras I (2013) The type VI secretion system encoded in SPI-6 plays a role in gastrointestinal colonization and systemic spread of Salmonella entericafserovar Typhimurium in the chicken. PLoS One 8:e63917

  8. Yang X, Huang J, Zhang Y, Liu S, Chen L, Xiao C, Zeng H, Wei X, Gu Q, Ying Li, Wang J, Ding Y, Zhang J, Wu Q (2020) Prevalence, abundance, serovars and antimicrobial resistance of Salmonella isolated from retail raw poultry meat in China. Total Environment 713:136385

    Article  CAS  Google Scholar 

  9. Rupiper DJ (1998) Diseases that affect race performance of homing pigeons. Part II: bacterial, fungal, and parasitic diseases. J Avian Med Surg 12:138–148

    Google Scholar 

  10. Kaczorek-Lukowska E, Sowinska P, Franaszek A, Dziewulska D, Malaczewska J, Stenzel T (2021) Can domestic pigeon be a potential carrier of zoonotic Salmonella? Transbound Emerg Dis 68(4):2321–2333

    Article  CAS  PubMed  Google Scholar 

  11. Brandao-Neto J, Stefan V, Mendonca BB, Bloise W, Castro AVB (1995) The essential role of zinc in growth. Nutr Res 15(3):335–358

    Article  CAS  Google Scholar 

  12. Nowak JE, Harmon K, Caldwell CC, Wong HR (2012) Prophylactic zinc supplementation reduces bacterial load and improves survival in a murine model of sepsis. Pediatr Crit Care Med 13(5):e323–e329

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wiegand S, Zakrzewski SS, Eichner M, Schulz E, Gunzel D, Pieper P, Rosenthal R, Barmeyer C, Bleich A, Dobrindt U, Schulzke JD, Bucker R (2017) Zinc treatment is efficient against Escherichia coli α-haemolysin-induced intestinal leakage in mice. Sci Rep 7:45649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Roy SK, Raqib R, Khatun W, Azim T, Chowdhury R, Fuchs GJ, Sack DA (2008) Zinc supplementation in the management of shigellosis in malnourished children in Bangladesh. Eur J Clin Nutr 62(7):849–855

    Article  CAS  PubMed  Google Scholar 

  15. Phatthalung PN, Min J, Wang F (2021) Macrophage-mediated defensive mechanisms involving zinc homeostasis in bacterial infection. Infectious Microbes & Diseases. https://doi.org/10.1097/IM9.0000000000000058

    Article  Google Scholar 

  16. Debski B (2016) Supplementation of pigs diet with zinc and copper as alternative to conventional antimicrobials. Pol J Vet Sci 19:917–924

    Article  CAS  PubMed  Google Scholar 

  17. Feldmann HR, Williams DR, Champagne JD, Lehenbauer TW, Aly SS (2019) Effectiveness of zinc supplementation on diarrhea and average daily gain in pre-weaned dairy calves: a double-blind, block-randomized placebo-controlled clinical trial. PLoS One 14(7):e0219321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Zhang B, Shao Y, Liu D, Yin P, Guo Y, 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 

  19. Shao Y, Lei Z, Yuan J, Yang Y, Guo Y, Zhang B (2014) Effect of zinc on growth performance, gut morphometry, and cecal microbial community in broilers challenged with Salmonella Typhimurium. J Microbiol 52:1002–1011

    Article  CAS  PubMed  Google Scholar 

  20. Oh HJ, Park YJ, Cho JH, Song MH, Gu BH, Yun W, Lee JH, An JS, Kim YJ, Lee JS, Kim S, Kim H, Kim ES, Lee BK, Kim BW, Kim HB, Cho JH, Kim MH (2021) Changes in diarrhea score, nutrient digestibility, zinc utilization, intestinal immune profiles, and fecal microbiome in weaned piglets by different forms of zinc. Animals (Basel) 11(5):1356

    Article  Google Scholar 

  21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  22. Sales J, Janssens GPJ (2003) Nutrition of the domestic pigeon (Columba livia domestica). World’s Poultry Science Journal 59:221–232

    Article  Google Scholar 

  23. Xie W, Fu Z, Pan N, Yan H, Wang X, Gao C (2019) Leucine promotes the growth of squabs by increasing crop milk protein synthesis through the TOR signaling pathway in the domestic pigeon (Columba livia). Poult Sci 98(11):5514–5524

    Article  CAS  PubMed  Google Scholar 

  24. Pasmans F, Baert K, Martel A, Bousquet-Melou A, Lanckriet R, De Boever S, Van Immerseel F, Eeckhaut V, de Backer P, Haesebrouck F (2008) Induction of the carrier state in pigeons infected with Salmonella enterica subspecies enterica serovar typhimurium PT99 by treatment with florfenicol: a matter of pharmacokinetics. Antimicrob Agents Chemother 52(3):954–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Finlay BB, Brumell JH (2000) Salmonella interactions with host cells: in vitro to in vivo. Philosophical Transactions of the Royal Society B: Biological Sciences 355(1397):623–631

    Article  CAS  Google Scholar 

  26. Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M, Kehl-Fie TE, Restrepo NA, Hosking MP, Edwards RA, Battistoni A, Pasquali P, Lane TE, Chazin WJ, Vogl T, Roth J, Skaar EP, Raffatellu M (2012) Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11:227–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Nickerson KP, Senger S, Zhang Y, Lima R, Patel S, Ingano L, Flavahan WA, Kumar DKV, Fraser CM (2018) Salmonella, typhi colonization provokes extensive transcriptional changes aimed at evading host mucosal immune defense during early infection of human intestinal tissue. EBioMedicine 31:92–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Reynolds JV (1996) Gut barrier function in the surgical patients. Br J Surg 83:1668–1671

    Article  CAS  PubMed  Google Scholar 

  29. Lamb-Rosteski JM, Kalischuk LD, Inglis GD, Buret AG (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  PubMed Central  Google Scholar 

  30. Hu C, Song J, Li Y, Luan Z, 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 

  31. Reddy EA, Shaw AV, Crump JA (2010) Community-acquired blood stream infections in Africa: a systematic review and meta-analysis. Lancet Infectious Diseases 10:417–432

    Article  PubMed  Google Scholar 

  32. Peterson DG, Scrimgeour AG, McClung JP, Koutsos EA (2008) Moderate zinc restriction affects intestinal health and immune function in lipopolysaccharide-challenged mice. J Nutr Biochem 19:193–199

    Article  CAS  PubMed  Google Scholar 

  33. Kim B, Lee WW (2021) Regulatory role of zinc in immune cell signaling. Moleculer Cells 44:335–341

    Article  CAS  Google Scholar 

  34. Monteith AJ, Skaar EP (2021) The impact of metal availability on immune function during infection. Trends Endocrinol Metab 32(11):916–928

    Article  CAS  PubMed  Google Scholar 

  35. Gordon S, Taylor P (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5:953–964

    Article  CAS  PubMed  Google Scholar 

  36. Singh S (2019) Zinc oxide nanoparticles impacts: cytotoxicity, genotoxicity, developmental toxicity, and neurotoxicity. Toxicol Mech Methods 29(4):300–311

    Article  CAS  PubMed  Google Scholar 

  37. Lei XJ, Kim IH (2020) Evaluation of coated zinc oxide in young pigs challenged with enterotoxigenic Escherichia coli K88. Animal Feed Science and Technology 262:114399

    Article  CAS  Google Scholar 

  38. Hasan R, Rink L, Haase H (2013) Zinc signals in neutrophil granulocytes are required for the formation of neutrophil extracellular traps. Innate Immun 19:253–264

    Article  PubMed  CAS  Google Scholar 

  39. Segal AW (2005) How neutrophils kill microbes. Annu Rev Immunol 23:197–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Brough D, Pelegrin P, Rothwell NJ (2009) Pannexin-1-dependent caspase-1 activation and secretion of IL-1beta is regulated by zinc. J Immunol 39:352–358

    CAS  Google Scholar 

  41. Holly MK, Han X, Zhao EJ, Crowley SM, Allaire JM, Knodler LA, Vallance BA, Smith JG (2020) Salmonella enterica infection of murine and human enteroid-derived monolayers elicits differential activation of epithelium intrinsic inflammasomes. Infect Immun 88:e00017-20

    Article  PubMed  PubMed Central  Google Scholar 

  42. Heckert RA, Estevez I, Russek-Cohen E, Pettit-Riley R (2002) Effects of density and perch availability on the immune status of broilers. Poult Sci 81:451–457

    Article  CAS  PubMed  Google Scholar 

  43. Ahiwe EU, Abdallh ME, Chang EP, Al-Qahtani M, Omede AA, Graham H, Iji PA (2019) Influence of autolyzed whole yeast and yeast components on broiler chickens challenged with salmonella lipopolysaccharide. Poult Sci 98:7129–7138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Cui H, Jing F, Xi P (2003) Pathology of the thymus, spleen and bursa of Fabricius in zinc-deficient ducklings. Avian pathology : journal of the WVPA 32:259–264

  45. Davis SK, Selva KJ, Kent SJ, Chung AW (2020) Serum IgA Fc effector functions in infectious disease and cancer. Immunology Cell Biology 98(4):276–286

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the Utility Fund of the Beijing Academy of Agriculture and Forestry Science under Grant [number: XMSSYJJ202004] and the innovation capacity building project of the Beijing Academy of Agriculture and Forestry Science under Grant [number: KJCX 20200404].

Funding

The Utility fund of Beijing Academy of Agriculture and Forestry Science,XMSSYJJ202004,Yuxin Shao,The Innovation capacity building project of Beijing Academy of Agriculture and Forestry Science,KJCX 20200404,Zheng Wang

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Authors and Affiliations

  1. Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China

    Zheng Wang, Xing Li, Shaohua Du, Xiaoshan Sun, Jianguo Huang & Yuxin Shao

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  1. Zheng Wang
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Contributions

Xing Li carried out the experiments. Shaohua Du, Xiaoshan Sun, and Jianguo Huang processed the data. Zheng Wang and Yuxin Shao designed the experiment and wrote the paper. The final manuscript was read and approved by all the authors.

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Correspondence to Yuxin Shao.

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Zheng Wang and Xing Li contributed equally to this work

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Wang, Z., Li, X., Du, S. et al. Protective Effects of Zinc on Salmonella Invasion, Intestinal Morphology and Immune Response of Young Pigeons Infected with Salmonella enterica Serovar Typhimurium. Biol Trace Elem Res 200, 4817–4827 (2022). https://doi.org/10.1007/s12011-021-03057-7

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