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Dietary High Sodium Fluoride Impairs Digestion and Absorption Ability, Mucosal Immunity, and Alters Cecum Microbial Community of Laying Hens

Miao, Liping, Zhu, Mingkun, Li, Huaiyu, Xu, Qianqian, Dong, Xinyang, Zou, Xiaoting·2020·Animals

Abstract

(1) Background: This study was conducted to investigate the effects of dietary fluoride (F) on tissue retention, digestive enzymes activities, mucosal immunity, and cecum microbial community of laying hens. (2) Methods: Total of 288 37-week-old Hy-Line Gray laying hens with similar laying rate (85.16% ± 3.87%) were adapted to the basal diets for ten days, and then allocated into three groups at random (n = 9, 6, 6 replicates/group). The concentrations of F in the diets were 31.19 (the control group, CON), 431.38 (F400, low-F group) and 1237.16 mg/kg (F1200, high-F group), respectively. The trial lasted for 59 days. (3) Results: Results suggested that F residuals in duodenum responded to dietary F concentrations positively. The activities of amylase, maltase and lactase were decreased in high-F group, compared with those in the control group. The mRNA expression levels of jejunum and ileum secretory immunoglobulin A (sIgA) and Mucin 2, and sIgA concentrations were decreased inhigh-F group, than those in the control group. The observed operational taxonomic units (OTUs) of laying hens in high-F group were higher than the CON and low-F groups, and the bacterial structure was different from the other two groups. The Lactobacillus was higher in the control group, while Gammaproteobacteria, Escherichia-Shigella, Streptococcaceae, and Enterobacteriaceae were higher in the high-F group. (4) Conclusions: The actual results confirmed that dietary high F intake increased the F residuals in duodenum, and reduced the digestion and absorption of nutrients and immunity via decreasing the activities of digestive enzymes, impairing intestine mucosal immunity, and disturbing the cecum microbial homeostasis of laying hens.

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Figure 1 Effects of dietary fluoride (F) level on the contents of F in the duodenum. Values were showed as the means and SD (n = 6). a–c Means with different superscript letters are significantly different (p < 0.05). CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.
Figure 1 Effects of dietary fluoride (F) level on the contents of F in the duodenum. Values were showed as the means and SD (n = 6). a–c Means with different superscript letters are significantly different (p < 0.05). CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.CC BY · PubMed Central
Figure 2 Effects of dietary fluoride levels on digestive enzyme activities of laying hens (n = 6). Values were showed as the means and SD (n = 6). a,b Means without common letters above the histogram differ significantly (p < 0.05). CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.
Figure 2 Effects of dietary fluoride levels on digestive enzyme activities of laying hens (n = 6). Values were showed as the means and SD (n = 6). a,b Means without common letters above the histogram differ significantly (p < 0.05). CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.CC BY · PubMed Central
Figure 3 Effect of dietary fluoride levels on the mRNA expression levels of sIgA and MUC2 in jejunum and ileum of laying hens (n = 6 in each group). Values were showed as the means and SD (n = 6). (a,b) Means without common letters above the histogram differ significantly (p < 0.05). sIgA, Secretory immunoglobulin A; MUC2, Mucin 2. CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.
Figure 3 Effect of dietary fluoride levels on the mRNA expression levels of sIgA and MUC2 in jejunum and ileum of laying hens (n = 6 in each group). Values were showed as the means and SD (n = 6). (a,b) Means without common letters above the histogram differ significantly (p < 0.05). sIgA, Secretory immunoglobulin A; MUC2, Mucin 2. CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.CC BY · PubMed Central
Figure 4 Effect of dietary fluoride levels on the contents of sIgA in jejunum and ileum of laying hens (n = 6 in each group). Values were showed as the means and SD (n = 6). (a–c) Mean without common letters above the histogram differ significantly (p < 0.05). sIgA, Secretory immunoglobulin A. CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.
Figure 4 Effect of dietary fluoride levels on the contents of sIgA in jejunum and ileum of laying hens (n = 6 in each group). Values were showed as the means and SD (n = 6). (a–c) Mean without common letters above the histogram differ significantly (p < 0.05). sIgA, Secretory immunoglobulin A. CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.CC BY · PubMed Central
Figure 5 Effects of dietary fluoride level on Venn diagram of cecal microbiota between groups (n = 5). Venn diagram was obtained at operational taxonomic units (OTUs) levels (97% similarity threshold). CON, the control group basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.
Figure 5 Effects of dietary fluoride level on Venn diagram of cecal microbiota between groups (n = 5). Venn diagram was obtained at operational taxonomic units (OTUs) levels (97% similarity threshold). CON, the control group basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.CC BY · PubMed Central
Figure 6 Effects of dietary fluoride level on the beta diversity of cecal microbiota between groups (n = 5). (A) nonmetric multidimensional scaling (NMDS) plot. (B) Clustering analysis. CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively
Figure 6 Effects of dietary fluoride level on the beta diversity of cecal microbiota between groups (n = 5). (A) nonmetric multidimensional scaling (NMDS) plot. (B) Clustering analysis. CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectivelyCC BY · PubMed Central
Figure 7 Cladogram representation of the differentially abundant families and genera (only top 50% are plotted here, n = 5). The root of the cladogram indicates the domain bacteria. The taxonomic levels of phylum and class are marked, while family and genus are abbreviated, with different colors indicating the group hosting the greatest abundance. The size of each node represents its relative abundance. CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.
Figure 7 Cladogram representation of the differentially abundant families and genera (only top 50% are plotted here, n = 5). The root of the cladogram indicates the domain bacteria. The taxonomic levels of phylum and class are marked, while family and genus are abbreviated, with different colors indicating the group hosting the greatest abundance. The size of each node represents its relative abundance. CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.CC BY · PubMed Central
Figure 8 Effects of dietary fluoride level on the relative abundance of intestinal opportunistic pathogen and beneficial bacteria in cecum of laying hens. Values are means ± SD (n = 5). a–b Means with different superscript letters are significantly different (p < 0.05). CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.
Figure 8 Effects of dietary fluoride level on the relative abundance of intestinal opportunistic pathogen and beneficial bacteria in cecum of laying hens. Values are means ± SD (n = 5). a–b Means with different superscript letters are significantly different (p < 0.05). CON, the control group, basal diet; F400 and F1200, diets supplemented with 400, and 1200 mg F/kg feed from sodium fluoride, respectively.CC BY · PubMed Central

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Research works printed but not linked: 42

  1. Schroder, 2003, Ecotoxicological risks associated with land treatment of petrochemical wastes. I. Residual soil contamination and bioaccumulation by cotton rats (Sigmodon hispidus), J. Toxicol. Environ., 66, 305
  2. Vithanage, 2015, Fluoride in the environment: Sources, distribution and defluoridation, Environ. Chem. Lett., 13, 131, 10.1007/s10311-015-0496-4 · DOI
  3. Yan, 2009, Effects of sodium fluoride treatment in vitro on cell proliferation, apoptosis and caspase-3 and caspase-9 mrna expression by neonatal rat osteoblasts, Arch. Toxicol., 83, 451, 10.1007/s00204-008-0365-z · DOI
  4. Zhang, 2017, Do Environmental Fluoride Exposure and ESRα Genetic Variation Modulate Methylation Modification on Bone Changes in Chinese Farmers?, Chem. Res. Toxicol., 30, 1302, 10.1021/acs.chemrestox.7b00047 · DOI
  5. Sharma, 2017, Fluoride: A review of pre-clinical and clinical studies, Environ. Toxicol. Pharmacol., 56, 297, 10.1016/j.etap.2017.10.008 · DOI
  6. Suzuki, 2017, Sirt1 overexpression suppresses fluoride-induced p53 acetylation to alleviate fluoride toxicity in ameloblasts responsible for enamel formation, Arch. Toxicol., 92, 1283, 10.1007/s00204-017-2135-2 · DOI
  7. Zhao, 2018, Fluoride induces apoptosis and autophagy through the IL-17 signaling pathway in mice hepatocytes, Arch. Toxicol., 92, 3277, 10.1007/s00204-018-2305-x · DOI
  8. Antonio, 2017, The effect of fluoride on the structure, function, and proteome of a renal epithelial cell monolayer, Environ. Toxicol., 32, 1455, 10.1002/tox.22338 · DOI
  9. Deng, 2016, Sodium fluoride (NaF) induces the splenic apoptosis via endoplasmic reticulum (ER) stress pathway in vivo and in vitro, Aging, 8, 3552, 10.18632/aging.101150 · DOI
  10. Sun, 2018, Alterations in epididymal proteomics and antioxidant activity of mice exposed to fluoride, Arch. Toxicol., 92, 169, 10.1007/s00204-017-2054-2 · DOI
  11. Wang, 2017, The MMP-9/TIMP-1 system is involved in fluoride-induced reproductive dysfunctions in female mice, Biol. Trace Elem. Res., 178, 253, 10.1007/s12011-016-0929-3 · DOI
  12. Luo, 2016, Dietary high fluorine alters intestinal microbiota in broiler chickens, Biol. Trace Elem. Res., 173, 483, 10.1007/s12011-016-0672-9 · DOI · Paper page
  13. Wang, 2019, Effect of Fluoride on Small Intestine Morphology and Serum Cytokine Contents in Rats, Biol. Trace Elem. Res., 189, 511, 10.1007/s12011-018-1503-y · DOI
  14. Gharzouli, 1994, Senator A Fluoride absorption in vitro by the gastrointestinal tract of the rat, Fluoride, 27, 185
  15. Mowat, 2014, Regional specialization within the intestinal immune system, Nat. Rev. Immunol., 14, 667, 10.1038/nri3738 · DOI
  16. 2007, Nutrition of the developing embryo and hatchling, Poult. Sci., 86, 1043, 10.1093/ps/86.5.1043 · DOI
  17. Noy, 2001, The effect of early feeding on growth and small intestinal development in the posthatch poult, Poult. Sci., 80, 912, 10.1093/ps/80.7.912 · DOI
  18. Potturi, 2005, Effects of delayed placement on intestinal characteristics in turkey poults, Poult. Sci., 84, 816, 10.1093/ps/84.5.816 · DOI
  19. Kau, 2011, Human nutrition, the gut microbiome and the immune system, Nature, 474, 327, 10.1038/nature10213 · DOI · Paper page
  20. Miao, 2017, Effects of excess dietary fluoride on serum biochemical indices, egg quality, and concentrations of fluoride in soft organs, eggs, and serum of laying hens, Biol. Trace Elem. Res., 180, 146, 10.1007/s12011-017-0973-7 · DOI
  21. Dong, 2017, Effects of dietary threonine supplementation on intestinal barrier function and gut microbiota of laying hens, Poult. Sci., 96, 3654, 10.3382/ps/pex185 · DOI
  22. Miao, 2019, Excess dietary fluoride affects laying performance, egg quality, tissue retention, serum biochemical indices, and reproductive hormones of laying hens, Poult. Sci., 98, 6873, 10.3382/ps/pez443 · DOI
  23. Youle, 2012, Mitochondrial fission, fusion, and stress, Science, 337, 1062, 10.1126/science.1219855 · DOI · Paper page
  24. Petit, 1995, Alterations in mitochondrial structure and function are early events of dexamethasone–induced thymocyte apoptosis, J. Cell Biol., 130, 157, 10.1083/jcb.130.1.157 · DOI
  25. Tu, 2018, Fluoride induces apoptosis via inhibiting SIRT1 activity to activate mitochondrial p53 pathway in human neuroblastoma SH-SY5Y cells, Toxicol. Appl. Pharmacol., 347, 60, 10.1016/j.taap.2018.03.030 · DOI
  26. Zhao, 2019, Roles of mitochondrial fission inhibition in developmental fluoride neurotoxicity: Mechanisms of action in vitro and associations with cognition in rats and children, Arch. Toxicol., 93, 709, 10.1007/s00204-019-02390-0 · DOI
  27. Valkonen, 2008, Effects of dietary energy content on the performance of laying hens in furnished and conventional cages, Poult. Sci., 87, 844, 10.3382/ps.2007-00237 · DOI
  28. Nochi, 2006, Innate immunity in themucosal immune system, Curr. Pharm. Des., 12, 4203, 10.2174/138161206778743457 · DOI
  29. Kim, 2010, Intestinal goblet cells and mucins in health and disease: Recent insights and progress, Curr. Gastroenterol. Rep., 12, 319, 10.1007/s11894-010-0131-2 · DOI
  30. Andrianifahanana, 2006, Regulation of mucin expression: Mechanistic aspects and implications for cancer and inflammatory diseases, Biochim. Biophys. Acta-Rev. Cancer, 1765, 189, 10.1016/j.bbcan.2006.01.002 · DOI
  31. Lillehoj, 1996, Avian gut-associated lymphoid tissues and intestinal immune responses to Eimeria parasites, Clin. Microbiol. Rev., 9, 349, 10.1128/CMR.9.3.349 · DOI
  32. Hosono, 2003, Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer’s patch cells, Biosci. Biotechnol. Biochem., 67, 758, 10.1271/bbb.67.758 · DOI
  33. Macpherson, 2001, IgA responses in the intestinal mucosa against pathogenic and non-pathogenic microorganisms, Microbes Infect., 3, 1021, 10.1016/S1286-4579(01)01460-5 · DOI
  34. Mascaraque, 2014, Intestinal inflammation and mucosal barrier function, Inflamm. Bowel Dis., 20, 2394, 10.1097/MIB.0000000000000204 · DOI
  35. Yan, 2017, Gut metagenomic analysis reveals prominent roles of Lactobacillus and cecal microbiota in chicken feed efficiency, Sci Rep., 7, 45308, 10.1038/srep45308 · DOI
  36. Million, 2012, Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals, Microb. Pathog., 53, 100, 10.1016/j.micpath.2012.05.007 · DOI
  37. Lowy, 1998, Staphylococcus aureus infections, N. Engl. J. Med., 339, 520, 10.1056/NEJM199808203390806 · DOI
  38. Collins, 2002, Streptococcus gallinaceus sp. nov., from chickens, Int. J. Syst. Evol. Microbiol., 52, 1161
  39. Feng, 2013, Near-infrared hyperspectral imaging and partial least squares regression for rapid and reagentless determination of Enterobacteriaceae on chicken fillets, Food Chem., 138, 1829, 10.1016/j.foodchem.2012.11.040 · DOI
  40. Athman, 2005, Shigella flexneri infection is dependent on villin in the mouse intestine and in primary cultures of intestinal epithelial cells, Cell Microbiol., 7, 1109, 10.1111/j.1462-5822.2005.00535.x · DOI
  41. Shi, R., Yang, X., Chen, L., Chang, H.T., Liu, H.Y., Zhao, J., Wang, X.W., and Wang, C.Q. (2014). Pathogenicity of Shigella in chickens. PLoS ONE, 9. · DOI
  42. Oakley, 2014, The chicken gastrointestinal microbiome, FEMS Microbiol. Lett., 360, 100, 10.1111/1574-6968.12608 · DOI

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Metadata

Authors
Miao, L., Zhu, M., Li, H., Xu, Q., Dong, X., & Zou, X.
Affiliations
Key Laboratory of Animal Feed and Nutrition of Zhejiang Province, Key Laboratory of Animal Nutrition and Feed Science in East China, Ministry of Agriculture, The Key Laboratory of Molecular Animal Nutrition, Ministry of Education, College of Animal Sciences, Zhejiang University, Hangzhou 310058, China
Venue
Animals
Publisher
MDPI AG
Published
2020-01-21
Volume
10
Issue
2
Pages
179
ISSN
2076-2615
Cited by
11
References
3
Language
en
Funders
the earmarked fund for Modern Argo-Industry Technology Research System of China (No. CARS-40-K10)

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CoChat. (2026). Citation check: Dietary High Sodium Fluoride Impairs Digestion and Absorption Ability, Mucosal Immunity, and Alters Cecum Microbial Community of Laying Hens. https://app.cochat.ai/papers/10.3390/ani10020179
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Miao, L., Zhu, M., Li, H., Xu, Q., Dong, X., & Zou, X. (2020). Dietary High Sodium Fluoride Impairs Digestion and Absorption Ability, Mucosal Immunity, and Alters Cecum Microbial Community of Laying Hens. Animals. https://doi.org/10.3390/ani10020179