Biological Trace Element Research

, Volume 155, Issue 2, pp 247–252 | Cite as

Effects of High Dietary Fluorine on Erythrocytes and Erythrocyte Immune Adherence Function in Broiler Chickens

  • Yubing Deng
  • Hengmin CuiEmail author
  • Xi Peng
  • Jing Fang
  • Zhicai Zuo
  • Junliang Deng
  • Qin Luo


Fluoride can exert toxic effects on soft tissues, giving rise to a broad array of symptoms and pathological changes. The aim of this study was to investigate on erythrocytes and erythrocyte immune adherence function in broiler chickens fed with high fluorine (F) diets by measuring the total erythrocyte count (TEC), the contents of hemoglobin (Hb), packed cell volumn (PCV), erythrocyte osmotic fragility (EOF), erythrocyte C3b receptor rosette rate (E-C3bRR), and erythrocyte immune complex rosette rate (E-ICRR). A total of 280 1-day-old healthy avian broiler chickens were randomly allotted into four equal groups of 70 birds each and fed with a corn–soybean basal diet containing 22.6 mg F/kg (control group) or same basal diets supplemented with 400, 800, and 1,200 mg F/kg (high F groups I, II, and III) in the form of sodium fluoride for 42 days. Blood samples were collected for the abovementioned parameters analysis at 14, 28, and 42 days of age during the experiment. The experimental results indicated that TEC, Hb, and PCV were significantly lower (p < 0.05 or p < 0.01), and EOF was higher (p < 0.05 or p < 0.01) in the high F groups II and III than that in the control group from 14 to 42 days of age. The E-C3bRR was significantly decreased (p < 0.01) in the three high F groups, whereas the E-ICRR was markedly increased (p < 0.01) in the high F groups II and III from 14 to 42 days of age. It was concluded that dietary F in the range of 800 to 1, 200 mg/kg could significantly cause anemia and impair the integrity of erythrocyte membrane, the transport capacity of oxygen and carbon dioxide, and erythrocyte immune adherence function in broiler chickens.


Broiler chicken EOF Erythrocyte immune adherence function Hb High dietary fluorine PCV TEC 



This research was supported by the program for Changjiang Scholars and the University Innovative Research Team (IRT 0848), and the Education Department of Sichuan Province (09ZZ017).


  1. 1.
    Møller IJ (1982) Fluorides and dental fluorosis. Int Dent J 32(2):135–147PubMedGoogle Scholar
  2. 2.
    Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Deng JL, Wang HS, Wu BY, Deng YX, Wang KP (2013) Decreased IgA + B cells population and IgA, IgG, IgM contents of the cecal tonsil induced by dietary high fluorine in broilers. Int J Environ Res Public Health 10(5):1775–1785PubMedCrossRefGoogle Scholar
  3. 3.
    Izuora K, Twombly JG, Whitford GM, Demertzis J, Pacifici R, Whyte MP (2011) Skeletal fluorosis from brewed tea. J Clin Endocrinol Metab 96(8):2318–2324PubMedCrossRefGoogle Scholar
  4. 4.
    Chinoy NJ, Sharma AK, Patel TN, Memon R, Jhala DD (2004) Recovery from fluoride and aluminium induced free radical liver toxicity in mice. Fluoride 37(4):257–263Google Scholar
  5. 5.
    Bai CM, Chen T, Cui Y, Gong T, Peng X, Cui HM (2010) Effect of high fluoride on the cell cycle and apoptosis of renal cells in chickens. Biol Trace Elem Res 138(1–3):173–180PubMedCrossRefGoogle Scholar
  6. 6.
    Chen T, Cui HM, Cui Y, Bai CM, Gong T (2011) Decreased antioxidase activities and oxidative stress in the spleen of chickens fed on high-fluorine diets. Hum Exp Toxicol 30(9):1282–1286PubMedCrossRefGoogle Scholar
  7. 7.
    Chen T, Cui HM, Cui Y, Bai CM, Gong T, Peng X (2011) Cell-cycle blockage associated with increased apoptotic cells in the thymus of chickens fed on diets high in fluorine. Hum Exp Toxicol 30(7):685–692PubMedCrossRefGoogle Scholar
  8. 8.
    Liu J, Cui HM, Peng X, Fang J, Zuo ZC, Wang HS, Wu BY, Deng YX, Wang KP (2012) High dietary fluorine induction of oxidative damage in the cecal tonsil of broilers. Fluoride 45(1):47–52Google Scholar
  9. 9.
    Ravichandran B, Chattopadhyay S, Gangopadhyay PK, Saiyed HN (2012) Evaluation of hematological changes in population exposed to fluoride. Toxicol Environ Chem 94(10):2052–2056CrossRefGoogle Scholar
  10. 10.
    Toghyani M, Tohidi M, Gheisari AA, Tabeidian SA (2010) Performance, immunity, serum biochemical and hematological parameters in broiler chicks fed dietary thyme as alternative for an antibiotic growth promote. Afr J Biotechnol 9(40):6819–6825Google Scholar
  11. 11.
    Samanta A, Bandyopadhyay B (2012) Effect of fluoride toxicity on some clinical, biochemical and physiological aspects of Albino rats. Res J Chem Environ 2:160–165Google Scholar
  12. 12.
    Uslu B (1981) Effects of fluoride on hemoglobin and hematocrit. Fluoride 14(1):38–41Google Scholar
  13. 13.
    Karadeniz A, Altintas L (2008) Effects of panax ginseng on fluoride-induced haematological pattern changes in mice. Fluoride 41(1):67–71Google Scholar
  14. 14.
    Mohiuddin SM, Reddy MV (1989) Haematological and biochemical studies on fluoride toxicity in sheep. Indian Vet J 66:1089–1091Google Scholar
  15. 15.
    Cetin N, Bilgili A, Eraslan G, Koyu A (2004) Effect of fluoride application on some blood parameters in rabbits. Eur J Health Sci 13:46–50Google Scholar
  16. 16.
    Khandare AL, Kumar PU, Lakshmaiah N (2000) Beneficial effect of tamarind ingestion on fluoride toxicity in dogs. Fluoride 33(1):33–38Google Scholar
  17. 17.
    Ersoy IH, Alanoglu EG, Koroglu BK, Varol S, Akcay S, Ugan Y, Ersoy S, Tamer MN (2010) Effect of endemic fluorosis on hematological parameters. Biol Trace Elem Res 138(1–3):22–27PubMedCrossRefGoogle Scholar
  18. 18.
    Swarup D, Dwivedi SK (2002) Environmental pollution and effects of lead and fluoride on animal health. Indian Council of Agricultural Research, New DelhiGoogle Scholar
  19. 19.
    Greer JP, Foerster J, Rodgers GM, Paraskevas F, Glader B, Arber DA, Means RT Jr (eds) (2009) Wintrobe's clinical hematology, 12th edn. Philadelphia, Lippincott Williams & WilkinsGoogle Scholar
  20. 20.
    Siegel I, Liu TL, Gleicher N (1981) The red-cell immune system. Lancet 318(8246):556–559CrossRefGoogle Scholar
  21. 21.
    Reinagel ML, Taylor RP (2000) Transfer of immune complexes from erythrocyte CR1 to mouse macrophages. J Immunol 164(4):1977–1985PubMedGoogle Scholar
  22. 22.
    Ali M (1990) Internal medicine, 2nd edn. Ilmi Kitab Khana, LahoreGoogle Scholar
  23. 23.
    Morera D, Mackenzie SA (2011) Is there a direct role for erythrocytes in the immune response? Vet Res 42(1):89PubMedCrossRefGoogle Scholar
  24. 24.
    Saralakumari D, Rao PR (1991) Red blood cell glucose metabolism in human chronic fluoride toxicity. Bull Environ Contam Toxicol 47(6):834–839PubMedCrossRefGoogle Scholar
  25. 25.
    Suska M, Lubkowska A (2007) The effect of environmental contamination with fluorine on the concentration of adenine nucleotides in the blood of black and white heifers. Polish J Environ Stud 16(3):441–445Google Scholar
  26. 26.
    Nabavi SM, Nabavi SF, Loizzo MR, Sureda A, Amani MA, Moghaddam AH (2012) Cytoprotective effect of silymarin against sodium fluoride-induced oxidative stress in rat erythrocytes. Fluoride 45(1):27–34Google Scholar
  27. 27.
    Agalakova NI, Gusev GP (2008) Diverse effects of fluoride on Na+ and K+ transport across the rat erythrocyte membrane. Fluoride 41(1):28–39Google Scholar
  28. 28.
    Rao MV, Vyas DD, Meda RB, Chawla SL (2011) In vitro protective role of melatonin against hemolysis induced by sodium fluoride in human red blood cells. Fluoride 44(2):77–82Google Scholar
  29. 29.
    Agalakova NI, Gusev GP (2011) Fluoride-induced death of rat erythrocytes in vitro. Toxicol In Vitro 25(8):1609–1618PubMedCrossRefGoogle Scholar
  30. 30.
    NRC (1994) Nutrient requirements of domestic animals. Nutrient requirements of poultry, 9th edn. National Academy of Science, Washington, DCGoogle Scholar
  31. 31.
    Ma HD (2004) Physiology experimental course. Sichuan Science and Technology, ChengduGoogle Scholar
  32. 32.
    Guo F, Qian BH, Zhang LZ (2002) Modern red blood cell immunology. Second Military Medical University Press, ShanghaiGoogle Scholar
  33. 33.
    Wintrobe MM (1974) Clinical hematology, 7th edn. Lea & Febiger, PhiladelphiaGoogle Scholar
  34. 34.
    Walker HK, Hall WD, Hurst JW, Eds (1990) Clinical methods: the history, physical, and laboratory examinations, 3rd ed. Butterworths, Boston. Chapter 151: Hemoglobin and hematocritGoogle Scholar
  35. 35.
    Tennant B, Harrold D, Reina-Guerra M, Kendrick JW, Laben RC (1974) Hematology of the neonatal calf: erythrocyte and leukocyte values of normal calves. Cornell Vet 64(4):516–532PubMedGoogle Scholar
  36. 36.
    Hoogstratten B, Leone NC, Shupe JL, Greenwood DA, Lieberman J (1965) Effect of fluorides on hematopoietic system, liver and thyroid gland in cattle. JAMA 192:26–32PubMedCrossRefGoogle Scholar
  37. 37.
    Hillman D, Bolenbaugh DL, Convey EM (1979) Hypothyroidism and anemia related to fluoride in dairy cattle. J Dairy Sci 62(3):416–423PubMedCrossRefGoogle Scholar
  38. 38.
    Balazova G, Macuch P, Rippel A (1969) Effects of fluorine emissions on the living organism. Flur Q Rep 2(1):33–36Google Scholar
  39. 39.
    Maiti SK, Das PK, Ray SK (2003) Effect of endemic fluorosis on haemogram of cattle and goat. Indian J Vet Med 23(1):34–37Google Scholar
  40. 40.
    Kolanjiappan K, Manoharan S, Kayalvizhi M (2002) Measurement of erythrocyte lipids, lipid peroxidation, antioxidants and osmotic fragility in cervical cancer patients. Clin Chim Acta 326(1–2):143–149PubMedCrossRefGoogle Scholar
  41. 41.
    O'Dell BL, Browning JD, Reeves PG (1987) Zinc deficiency increases the osmotic fragility of rat erythrocytes. J Nutr 117(11):1883–1889PubMedGoogle Scholar
  42. 42.
    Weed RI, Bowdler AJ (1966) Metabolic dependence of the critical hemolytic volume of human erythrocytes: relationship to osmotic fragility and autohemolysis in hereditary spherocytosis and normal red cells. J Clin Invest 45(7):1137–1149PubMedCrossRefGoogle Scholar
  43. 43.
    Kim J, Borges WH, Holliday MA (1962) Correlation between RBC osmotic fragility and serum sodium. Am J Dis Child 104:281–288PubMedGoogle Scholar
  44. 44.
    Bogin E, Massry SG, Levi J, Djaldeti M, Bristol G, Smith J (1982) Effect of parathyroid hormone on osmotic fragility of human erythrocytes. J Clin Invest 69(4):1017–1025PubMedCrossRefGoogle Scholar
  45. 45.
    Ambali SF, Ayo JO, Ojo SA, Esievo KA (2011) Ameliorative effect of vitamin C on chronic chlorpyrifos-induced erythrocyte osmotic fragility in Wistar rats. Hum Exp Toxicol 30(1):19–24PubMedCrossRefGoogle Scholar
  46. 46.
    Adenkola AY, Ayo JO (2009) Effect of road transportation on erythrocyte osmotic fragility of pigs administered ascorbic acid during the harmattan season in Zaria, Nigeria. J Cell Anim Biol 3(1):4–8Google Scholar
  47. 47.
    Brzezińska-Slebodzińska E (2001) Erythrocyte osmotic fragility test as the measure of defence against free radicals in rabbits of different age. Acta Vet Hung 49(4):413–419PubMedCrossRefGoogle Scholar
  48. 48.
    Ranjan R, Swarup D, Patra RC (2009) Oxidative stress indices in erythrocytes, liver, and kidneys of fluoride-exposed rabbits. Fluoride 42(2):88–93Google Scholar
  49. 49.
    Yur F, Belge F, Mert N, Yörük I (2003) Changes in erythrocyte parameters of fluorotic sheep. Fluoride 36(3):152–156Google Scholar
  50. 50.
    Mudad R, Telen MJ (1996) Biologic functions of blood group antigens. Curr Opin Hematol 3(6):473–479PubMedCrossRefGoogle Scholar
  51. 51.
    Birmingham DJ, Hebert LA (2001) CR1 and CRl-like: the primate immune adherence receptors. Immunol Rev 180(1):100–111PubMedCrossRefGoogle Scholar
  52. 52.
    Zhu YZ, Zhao HS, Li XW, Zhang LC, Hu CW, Shao B, Sun H, Bah AA, Li YF, Zhang ZG (2011) Effects of subchronic aluminum exposure on the immune function of erythrocytes in rats. Biol Trace Elem Res 143(3):1576–1580PubMedCrossRefGoogle Scholar
  53. 53.
    Oudin S, Libyh MT, Goossens D, Dervillez X, Philbert F, Réveil B, Bougy F, Tabary T, Rouger P, Klatzmann D et al (2000) A soluble recombinant multimeric anti-RH(D) single-chain Fv/CR1 molecule restores the immune complex binding ability of CR1-deficient erythrocytes. J Immunol 164(3):1505–1513PubMedGoogle Scholar
  54. 54.
    Jiang JB, Wu CH, Gao H, Song JD, Li HQ (2010) Effects of astragalus polysaccharides on immunologic function of erythrocyte in chickens infected with infectious bursa disease virus. Vaccine 28(34):5614–5616PubMedCrossRefGoogle Scholar
  55. 55.
    Okada K, Brown EJ (1988) Sodium fluoride reveals multiple pathways for regulation of surface expression of the C3b/C4b receptor (CR1) on human polymorphonuclear leukocytes. J Immunol 140(3):878–884PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Yubing Deng
    • 1
  • Hengmin Cui
    • 1
    Email author
  • Xi Peng
    • 1
  • Jing Fang
    • 1
  • Zhicai Zuo
    • 1
  • Junliang Deng
    • 1
  • Qin Luo
    • 1
  1. 1.Key Laboratory of Animal Diseases and Environmental Hazards of Sichuan Province, College of Veterinary MedicineSichuan Agricultural UniversityYa’anChina

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