Advertisement

Selenium Deficiency in Chickens Induces Intestinal Mucosal Injury by Affecting the Mucosa Morphology, SIgA Secretion, and GSH-Px Activity

  • Xianjing He
  • Yucai Lin
  • Shuai Lian
  • Dongbo Sun
  • Donghua Guo
  • Jianfa WangEmail author
  • Rui WuEmail author
Article
  • 40 Downloads

Abstract

The small intestine is one of the target organs of dietary selenium (Se) deficiency. Our objective was to investigate the effects of Se deficiency on small intestinal mucosa morphology and function in chickens. In the present study, 1-day (d)-old chickens were fed either a commercial diet with 0.15 mg/kg Se (control group) or a Se-deficient diet with 0.016 mg/kg Se (Se-group). The average daily weight gain, Se content in the blood, secretory immunoglobulin A (SIgA) secretion, and glutathione peroxidase (GSH-Px) activity in the small intestine in chickens were examined after 10, 20, 30, and 40 days of feeding. We also observed the morphology of the small intestine and recorded the number of intraepithelial lymphocytes (IELs). The average daily weight gain decreased; the level of Se in the blood decreased significantly; and SIgA secretion and GSH-Px activity in the duodenum, jejunum, and ileum decreased to different degrees. Histological analysis showed that the villus length, crypt depth, mucosal thickness, and number of IELs in the small intestine decreased to different extents in different periods. In the Se-group, longer feeding times were associated with more severe injury to physiological structure and function in the intestinal mucosa in chickens. In conclusion, Se deficiency induced injury of the mucosal immune barrier and physical barrier of the small intestine, and decreased the growth performance and antioxidant capacity in chickens.

Keywords

Selenium deficiency Chicken Small intestine Mucosal immunity 

Notes

Funding Information

This work was financially supported by the National Natural Science Foundation of China (grant 31272624) and Heilongjiang Bayi Agricultural University Support Program for San Heng San Zong (ZRCQC201903).

Compliance with Ethical Standards

All procedures used in this study were approved by the Institutional Animal Care and Use Committee of Heilongjiang Bayi Agricultural University.

Conflict of Interest

The authors declare that they have no competing interests.

References

  1. 1.
    Schwarz K, Fredga A (1975) Biological potency of organic selenium compounds: VI. Aliphatic seleninic acids and carboxyselenic acids. Bioinorg Chem 4(3):235–243.  https://doi.org/10.1016/s0006-3061(00)80106-4 CrossRefPubMedGoogle Scholar
  2. 2.
    Schwarz K, Porter LA, Fredga A (1974) Biological potency of organic selenium compounds. IV Straight-chain dialkylmono- and diselenides. Bioinorganic chemistry 3(2):145–152CrossRefGoogle Scholar
  3. 3.
    Kim Y, Kim DC, Cho ES, Ko SO, Kwon WY, Suh GJ, Shin HK (2014) Antioxidant and anti-inflammatory effects of selenium in oral buccal mucosa and small intestinal mucosa during intestinal ischemia-reperfusion injury. Journal of inflammation (London, England) 11(1):36.  https://doi.org/10.1186/s12950-014-0036-1 CrossRefGoogle Scholar
  4. 4.
    Kim KS, Suh GJ, Kwon WY, Kwak YH, Lee K, Lee HJ, Jeong KY, Lee MW (2012) Antioxidant effects of selenium on lung injury in paraquat intoxicated rats. Clinical toxicology (Philadelphia, Pa) 50(8):749–753.  https://doi.org/10.3109/15563650.2012.708418 CrossRefGoogle Scholar
  5. 5.
    Ozbal S, Erbil G, Kocdor H, Tugyan K, Pekcetin C, Ozogul C (2008) The effects of selenium against cerebral ischemia-reperfusion injury in rats. Neurosci Lett 438(3):265–269.  https://doi.org/10.1016/j.neulet.2008.03.091 CrossRefPubMedGoogle Scholar
  6. 6.
    Tsuji PA, Carlson BA, Anderson CB, Seifried HE, Hatfield DL, Howard MT (2015) Dietary selenium levels affect selenoprotein expression and support the interferon-gamma and IL-6 immune response pathways in mice. Nutrients 7(8):6529–6549.  https://doi.org/10.3390/nu7085297 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Combs GF Jr (2015) Biomarkers of selenium status. Nutrients 7(4):2209–2236.  https://doi.org/10.3390/nu7042209 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Kiremidjian-Schumacher L, Roy M, Wishe HI, Cohen MW, Stotzky G (1990) Selenium and immune cell functions. I. Effect on lymphocyte proliferation and production of interleukin 1 and interleukin 2. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine (New York, NY) 193(2):136–142.  https://doi.org/10.3181/00379727-193-43014 CrossRefGoogle Scholar
  9. 9.
    Navarro-Alarcon M, Lopez-Martinez MC (2000) Essentiality of selenium in the human body: relationship with different diseases. Sci Total Environ 249(1–3):347–371.  https://doi.org/10.1016/s0048-9697(99)00526-4 CrossRefPubMedGoogle Scholar
  10. 10.
    Pappas AC, Zoidis E, Surai PF, Zervas G (2008) Selenoproteins and maternal nutrition. Comparative biochemistry and physiology Part B, Biochemistry & molecular biology 151(4):361–372.  https://doi.org/10.1016/j.cbpb.2008.08.009 CrossRefGoogle Scholar
  11. 11.
    Surai PF (2000) Effect of selenium and vitamin E content of the maternal diet on the antioxidant system of the yolk and the developing chick. Br Poult Sci 41(2):235–243.  https://doi.org/10.1080/713654909 CrossRefPubMedGoogle Scholar
  12. 12.
    Yildirim S, Ozkan C, Huyut Z, Cinar A (2019) Detection of Se, vit. E, vit. A, MDA, 8-OHdG, and CoQ10 levels and histopathological changes in heart tissue in sheep with white muscle disease. Biol Trace Elem Res 188(2):419–423.  https://doi.org/10.1007/s12011-018-1434-7 CrossRefPubMedGoogle Scholar
  13. 13.
    Wang J, Lian S, He X, Yu D, Liang J, Sun D, Wu R (2018) Selenium deficiency induces splenic growth retardation by deactivating the IGF-1R/PI3K/Akt/mTOR pathway. Metallomics : integrated biometal science 10(11):1570–1575.  https://doi.org/10.1039/c8mt00183a CrossRefGoogle Scholar
  14. 14.
    Baldwin AL, Wiley EB (2002) Selenium reduces hemoglobin-induced epithelial damage to intestinal mucosa. Artif Cells Blood Substit Immobil Biotechnol 30(1):1–22CrossRefGoogle Scholar
  15. 15.
    Baldwin AL, Wiley EB, Summers AG, Alayash AI (2003) Sodium selenite reduces hemoglobin-induced venular leakage in the rat mesentery. Am J Phys Heart Circ Phys 284(1):H81–H91.  https://doi.org/10.1152/ajpheart.00562.2002 CrossRefGoogle Scholar
  16. 16.
    Teige J, Tollersrud S, Lund A, Larsen HJ (1982) Swine dysentery: the influence of dietary vitamin E and selenium on the clinical and pathological effects of Treponema hyodysenteriae infection in pigs. Res Vet Sci 32(1):95–100CrossRefGoogle Scholar
  17. 17.
    Massironi S, Rossi RE, Cavalcoli FA, Della Valle S, Fraquelli M, Conte D (2013) Nutritional deficiencies in inflammatory bowel disease: therapeutic approaches. Clinical nutrition (Edinburgh, Scotland) 32(6):904–910.  https://doi.org/10.1016/j.clnu.2013.03.020 CrossRefGoogle Scholar
  18. 18.
    Clark LC, Combs GF Jr, Turnbull BW, Slate EH, Chalker DK, Chow J, Davis LS, Glover RA, Graham GF, Gross EG, Krongrad A, Lesher JL Jr, Park HK, Sanders BB Jr, Smith CL, Taylor JR (1996) Effects of selenium supplementation for cancer prevention in patients with carcinoma of the skin. A randomized controlled trial. Nutritional Prevention of Cancer Study Group. Jama 276(24):1957–1963CrossRefGoogle Scholar
  19. 19.
    Peters U, Chatterjee N, Church TR, Mayo C, Sturup S, Foster CB, Schatzkin A, Hayes RB (2006) High serum selenium and reduced risk of advanced colorectal adenoma in a colorectal cancer early detection program. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 15(2):315–320.  https://doi.org/10.1158/1055-9965.epi-05-0471 CrossRefGoogle Scholar
  20. 20.
    Davis CD, Uthus EO (2003) Dietary folate and selenium affect dimethylhydrazine-induced aberrant crypt formation, global DNA methylation and one-carbon metabolism in rats. J Nutr 133(9):2907–2914.  https://doi.org/10.1093/jn/133.9.2907 CrossRefPubMedGoogle Scholar
  21. 21.
    Baines AT, Holubec H, Basye JL, Thorne P, Bhattacharyya AK, Spallholz J, Shriver B, Cui H, Roe D, Clark LC, Earnest DL, Nelson MA (2000) The effects of dietary selenomethionine on polyamines and azoxymethane-induced aberrant crypts. Cancer Lett 160(2):193–198.  https://doi.org/10.1016/s0304-3835(00)00585-1 CrossRefPubMedGoogle Scholar
  22. 22.
    Feng Y, Finley JW, Davis CD, Becker WK, Fretland AJ, Hein DW (1999) Dietary selenium reduces the formation of aberrant crypts in rats administered 3,2′-dimethyl-4-aminobiphenyl. Toxicol Appl Pharmacol 157(1):36–42.  https://doi.org/10.1006/taap.1999.8623 CrossRefPubMedGoogle Scholar
  23. 23.
    Wang J, Liu Z, He X, Lian S, Liang J, Yu D, Sun D, Wu R (2018) Selenium deficiency induces duodenal villi cell apoptosis via an oxidative stress-induced mitochondrial apoptosis pathway and an inflammatory signaling-induced death receptor pathway. Metallomics : integrated biometal science 10(10):1390–1400.  https://doi.org/10.1039/c8mt00142a CrossRefGoogle Scholar
  24. 24.
    Barrett CW, Singh K, Motley AK, Lintel MK, Matafonova E, Bradley AM, Ning W, Poindexter SV, Parang B, Reddy VK, Chaturvedi R, Fingleton BM, Washington MK, Wilson KT, Davies SS, Hill KE, Burk RF, Williams CS (2013) Dietary selenium deficiency exacerbates DSS-induced epithelial injury and AOM/DSS-induced tumorigenesis. PLoS One 8(7):e67845.  https://doi.org/10.1371/journal.pone.0067845 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Hasunuma R, Ogawa T, Kawanishi Y (1982) Fluorometric determination of selenium in nanogram amounts in biological materials using 2,3-diaminonaphthalene. Anal Biochem 126(2):242–245.  https://doi.org/10.1016/0003-2697(82)90510-3 CrossRefPubMedGoogle Scholar
  26. 26.
    Zhu Y, Guan Y, Loor JJ, Sha X, Coleman DN, Zhang C, Du X, Shi Z, Li X, Wang Z (2019) Fatty acid-induced endoplasmic reticulum stress promoted lipid accumulation in calf hepatocytes, and endoplasmic reticulum stress existed in the liver of severe fatty liver cows. J Dairy SciGoogle Scholar
  27. 27.
    Tsuji PA, Carlson BA, Yoo MH, Naranjo-Suarez S, Xu XM, He Y, Asaki E, Seifried HE, Reinhold WC, Davis CD, Gladyshev VN, Hatfield DL (2015) The 15kDa selenoprotein and thioredoxin reductase 1 promote colon cancer by different pathways. PLoS One 10(4):e0124487.  https://doi.org/10.1371/journal.pone.0124487 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Barrett CW, Reddy VK, Short SP, Motley AK, Lintel MK, Bradley AM, Freeman T, Vallance J, Ning W, Parang B, Poindexter SV, Fingleton B, Chen X, Washington MK, Wilson KT, Shroyer NF, Hill KE, Burk RF, Williams CS (2015) Selenoprotein P influences colitis-induced tumorigenesis by mediating stemness and oxidative damage. J Clin Invest 125(7):2646–2660.  https://doi.org/10.1172/jci76099 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Mseddi M, Ben Mansour R, Mnif F, Gargouri B, Abid M, Guermazi F, Attia H, Lassoued S (2015) Lipid peroxidation, proteins modifications, anti-oxidant enzymes activities and selenium deficiency in the plasma of hashitoxicosis patients. Therapeutic advances in endocrinology and metabolism 6(5):181–188.  https://doi.org/10.1177/2042018815589057 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Fang LQ, Goeijenbier M, Zuo SQ, Wang LP, Liang S, Klein SL, Li XL, Liu K, Liang L, Gong P, Glass GE, van Gorp E, Richardus JH, Ma JQ, Cao WC, de Vlas SJ (2015) The association between hantavirus infection and selenium deficiency in mainland China. Viruses 7(1):333–351.  https://doi.org/10.3390/v7010333 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Burk RF (1987) Production of selenium deficiency in the rat. Methods Enzymol 143:307–313.  https://doi.org/10.1016/0076-6879(87)43058-9 CrossRefPubMedGoogle Scholar
  32. 32.
    Thompson JN, Scott ML (1969) Role of selenium in the nutrition of the chick. J Nutr 97(3):335–342.  https://doi.org/10.1093/jn/97.3.335 CrossRefPubMedGoogle Scholar
  33. 33.
    Yin F, Sancheti H, Cadenas E (2012) Mitochondrial thiols in the regulation of cell death pathways. Antioxid Redox Signal 17(12):1714–1727.  https://doi.org/10.1089/ars.2012.4639 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lin SL, Wang CW, Tan SR, Liang Y, Yao HD, Zhang ZW, Xu SW (2014) Selenium deficiency inhibits the conversion of thyroidal thyroxine (T4) to triiodothyronine (T3) in chicken thyroids. Biol Trace Elem Res 161(3):263–271.  https://doi.org/10.1007/s12011-014-0083-8 CrossRefPubMedGoogle Scholar
  35. 35.
    Zhao X-J, Li Z-P, Wang J-H, Xing X-M, Wang Z-Y, Wang L, Wang Z-H (2015) Effects of chelated Zn/Cu/Mn on redox status, immune responses and hoof health in lactating Holstein cows. J Vet Sci 16(4):439–446CrossRefGoogle Scholar
  36. 36.
    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(1):105–114.  https://doi.org/10.1080/00071668.2013.873772 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  1. 1.College of Animal Science and Veterinary MedicineHeilongjiang Bayi Agricultural UniversityDaqingPeople’s Republic of China
  2. 2.College of Agriculture and Animal Husbandry EngineeringHeilongjiang PolytechnicHarbinPeople’s Republic of China

Personalised recommendations