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Effects of Dietary Supplementation with Iron in Breeding Pigeons on the Blood Iron Status, Tissue Iron Content, and Full Expression of Iron-Containing Enzymes of Squabs

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Abstract

This study was aimed at investigating the effects of diet iron levels on the blood iron status, tissue iron content, mRNA levels, and the activity of iron-containing enzymes in different tissues of squabs. A total of 120 pairs of healthy Silver Feather King parental pigeons with similar average body weight and egg production were randomly divided into 5 groups with 8 replicates and 3 pairs of pigeons per replicate. The five groups of breeding pigeons were fed an iron-unsupplemented basal diet and basal diet supplemented with 75, 150, 300, and 600 mg iron/kg, respectively. The diets were fed in the form of granular feed based on corn, soybean meal, wheat, and sorghum. A broken line model was used for regression analysis. The results showed that plasma iron (PI), serum ferritin, iron contents in crop milk and liver, liver catalase (CAT) activity, and heart succinate dehydrogenase (SDH) activity were affected by iron levels (P < 0.05). And PI, serum ferritin, iron content in crop milk, and heart SDH activity increased quadratically (P < 0.05), but the iron content and CAT activity in the liver decreased quadratically (P < 0.005) as dietary iron level increased. According to the broken-line model of serum ferritin fitting (P < 0.002), the optimal dietary iron level of breeding pigeons was estimated to be 193 mg/kg. In conclusion, serum ferritin is a sensitive index to evaluate the iron requirement of the breeding pigeon with two squabs, and the recommended iron supplemental level is 193 mg/kg.

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

References

  1. Ji F, Zhang D, Shao Y, Yu X, Liu X, Shan D, Wang Z (2020) Changes in the diversity and composition of gut microbiota in pigeon squabs infected with Trichomonas Gallinae. Sci Rep 10(1):19978. https://doi.org/10.1038/s41598-020-76821-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Xu Q, Li H, Zhou W, Zou X, Dong X (2020) Age-related changes in serum lipid levels, hepatic morphology, antioxidant status, lipid metabolism related gene expression and enzyme activities of domestic pigeon squabs (Columba Livia). Animals (Basel) 10(7):1121. https://doi.org/10.3390/ani10071121

    Article  PubMed  Google Scholar 

  3. 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. https://doi.org/10.3382/ps/pez296

    Article  CAS  PubMed  Google Scholar 

  4. Chen M, Fu Z, Jiang S, Wang X, Yan H, Gao C (2020) Targeted disruption of TORC1 retards young squab growth by inhibiting the synthesis of crop milk protein in breeding pigeon (Columba Livia). Poult Sci 99(1):416–422. https://doi.org/10.3382/ps/pez513

    Article  CAS  PubMed  Google Scholar 

  5. Shao Y, Ma W, Ji F, Sun X, Du S, Li X, Li Q, Wang Z (2021) Exploration of proteomics analysis of crop milk in pigeons (Columba livia) during the lactation period. ACS Omega 6(42):27726–27736. https://doi.org/10.1021/acsomega.1c02977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Xu Q, Wen J, Wang X, Zou X, Dong X (2021) Maternal dietary linoleic acid altered intestinal barrier function in domestic pigeons (Columba livia). Br J Nutr 126(7):1003–1016. https://doi.org/10.1017/S0007114520004973

    Article  CAS  PubMed  Google Scholar 

  7. Ji F, Zhang S, An Y, Wang Z, Shao Y, Du S, Li X, Sun X (2022) Influence of dietary phosphorus concentrations on the performance of rearing pigeons (Columba livia), and bone properties of squabs. Poult Sci 101(4):101744. https://doi.org/10.1016/j.psj.2022.101744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Chang L, Zhang R, Fu S, Mu C, Tang Q, Bu Z (2019) Effects of different dietary calcium levels on the performance, egg quality, and albumen transparency of laying pigeons. Animals (Basel) 9(3):110. https://doi.org/10.3390/ani9030110

    Article  PubMed  Google Scholar 

  9. Qin Z, Caruso J, Lai B, Matusch A, Becker J (2011) Trace metal imaging with high spatial resolution: applications in biomedicine. Metallomics 3(1):28–37. https://doi.org/10.1039/c0mt00048e

    Article  CAS  PubMed  Google Scholar 

  10. Wang W, Di X, D’agostino R, Torti S, Torti F (2007) Excess capacity of the iron regulatory protein system. J Biol Chem 282(34):24650–24659. https://doi.org/10.1074/jbc.M703167200

    Article  CAS  PubMed  Google Scholar 

  11. Taschetto D, Vieira S, Angel C, Stefanello C, Kindlein L, Ebbing M, Simões C (2017) Iron requirements of broiler breeder hens. Poult Sci 96(11):3920–3927. https://doi.org/10.3382/ps/pex208

    Article  CAS  PubMed  Google Scholar 

  12. Tan Z, Lu P, Adewole D, Diarra MS, Gong J, Yang C (2020) Iron requirement in the infection of Salmonella and its relevance to poultry health. J Appl Poult Res 30(1):100101. https://doi.org/10.1016/j.japr.2020.09.016

    Article  CAS  Google Scholar 

  13. Baker R, Greer F (2010) Diagnosis and prevention of iron deficiency and iron-deficiency anemia in infants and young children (0–3 Years of Age). Pediatrics 126(5):1040–1050. https://doi.org/10.1542/peds.2010-2576

    Article  PubMed  Google Scholar 

  14. Zhang B, Sui F, Wang B, Wang Y, Li W (2020) Dietary combined supplementation of iron and Bacillus subtilis enhances reproductive performance, eggshell quality, nutrient digestibility, antioxidant capacity, and hematopoietic function in breeder geese. Poult Sci 99(11):6119–6127. https://doi.org/10.1016/j.psj.2020.06.077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. National Research Council (1994) Nutrient requirements for poultry, 9th rev. edn. National Academies Press, Washington, D.C. https://doi.org/10.17226/2114

    Book  Google Scholar 

  16. Yousefi A, Saki A (2019) Iron loaded chitooligosaccharide nanoparticles reduces incidence of bacterial chondronecrosis with osteomyelitis in broiler chickens. Iran J Appl Anim Sci 9(2):329–336

    CAS  Google Scholar 

  17. Behroozlak MA, Daneshyar M, Farhoomand P, Nikoo A (2019) Effect of replacing dietary FeSO4 with FeHPO4 nanoparticles on growth performance, carcass characteristics and tissue iron content in broilers. Iran J Appl Anim Sci 9(4):709–716

    CAS  Google Scholar 

  18. Hagler L, Askew E, Neville J, Mellick P, Coppes R, Lowder JF (1981) Influence of dietary iron deficiency on hemoglobin, myoglobin, their respective reductases, and skeletal muscle mitochondrial respiration. Am J Clin Nutr 34(10):2169–2177. https://doi.org/10.1093/ajcn/34.10.2169

    Article  CAS  PubMed  Google Scholar 

  19. Siimes M, Refino C, Dallman P (1980) Manifestation of iron deficiency at various levels of dietary iron intake. Am J Clin Nutr 33(3):570–574. https://doi.org/10.1093/ajcn/33.3.570

    Article  CAS  PubMed  Google Scholar 

  20. Liao X, Ma C, Lu L, Zhang L, Luo X (2017) Determination of dietary iron requirements by full expression of iron-containing cytochrome c oxidase in the heart of broilers from 22 to 42 d of age. Br J Nutr 118(7):493–499. https://doi.org/10.1017/S0007114517002458

    Article  CAS  PubMed  Google Scholar 

  21. de Deungria M, Rao R, Wobken JD, Luciana M, Nelson CA, Georgieff MK (2000) Perinatal iron deficiency decreases cytochrome c oxidase (cytox) activity in selected regions of neonatal rat brain. Pediatr Res 48(2):169–76. https://doi.org/10.1203/00006450-200008000-00009

    Article  CAS  PubMed  Google Scholar 

  22. Feng J, Ma W, Xu Z, He J, Wang Y, Liu J (2008) The effect of iron glycine chelate on tissue mineral levels, fecal mineral concentration, and liver antioxidant enzyme activity in weanling pigs. Anim Feed Sci Technol 150(1):106–113. https://doi.org/10.1016/j.anifeedsci.2008.07.004

    Article  CAS  Google Scholar 

  23. Ma X, Liao X, Lu L, Li S, Zhang L, Luo X (2016) Determination of dietary iron requirements by full expression of iron-containing enzymes in various tissues of broilers. J Nutr 146(11):2267–2273. https://doi.org/10.3945/jn.116.237750

    Article  CAS  PubMed  Google Scholar 

  24. Zhao D, Li X, Wang Z, Shi Z, Qin S, Shao Y, Sun X, Zhang X (2022) Effects of different levels of iron in breeding pigeon diet on body weight, slaughter performance, meat quality and blood indexes of pigeons. Chin J Anim Nutr 34(6):3635–3644

    CAS  Google Scholar 

  25. Tran H, Schlageter-Tello A, Caprez A, Miller PS, Hall MB, Weiss WP, Kononoff PJ (2020) Development of feed composition tables using a statistical screening procedure. J Dairy Sci 103(4):3786–3803. https://doi.org/10.3168/jds.2019-16702

    Article  CAS  PubMed  Google Scholar 

  26. Huebers H, Eng M, Josephson B, Ekpoom N, Rettmer R, Labbé R, Pootrakul P, Finch CA (1987) Plasma iron and transferrin iron-binding capacity evaluated by colorimetric and immunoprecipitation methods. Clin Chem 33(2):273–277. https://doi.org/10.1093/clinchem/33.2.273

    Article  CAS  PubMed  Google Scholar 

  27. Anon (1978) The measurement of total and unsaturated iron-binding capacity in serum. Br J Haematol 38(2):281–287. https://doi.org/10.1111/j.1365-2141.1978.tb01044.x

    Article  Google Scholar 

  28. Huang Y, Lu L, Luo X, Liu B (2007) An optimal dietary zinc level of broiler chicks fed a corn-soybean meal diet. Poult Sci 86(12):2582–2589. https://doi.org/10.3382/ps.2007-00088

    Article  CAS  PubMed  Google Scholar 

  29. Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(t)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  30. Nulton-Persson A, Szweda L (2001) Modulation of mitochondrial function by hydrogen peroxide. J Biol Chem 276(26):23357–23361. https://doi.org/10.1074/jbc.M100320200

    Article  CAS  PubMed  Google Scholar 

  31. Hou H, Li B, Zhao X, Zhuang Y, Ren G, Yan M, Cai Y, Zhang X, Chen L (2009) The effect of pacific cod (Gadus Macrocephalus) skin gelatin polypeptides on UV radiation-induced skin photoaging in ICR mice. Food Chem 115(3):945–950. https://doi.org/10.1016/j.foodchem.2009.01.015

    Article  CAS  Google Scholar 

  32. Lu L, Chang B, Liao X, Wang R, Zhang L, Luo X (2016) Use of molecular biomarkers to estimate manganese requirements for broiler chickens from 22 to 42 d of age. Br J Nutr 116(9):1512–1518. https://doi.org/10.1017/S0007114516003640

    Article  CAS  PubMed  Google Scholar 

  33. Robbins KR, Norton HW, Baker DH (1979) Estimation of nutrient requirements from growth data. J Nutr 109(10):1710–4. https://doi.org/10.1093/jn/109.10.1710

    Article  CAS  PubMed  Google Scholar 

  34. Corzo A, Dozier W, Kidd M (2006) Dietary lysine needs of late-developing heavy broilers. Poult Sci 85(3):457–461. https://doi.org/10.1093/ps/85.3.457

    Article  CAS  PubMed  Google Scholar 

  35. Bainton D, Finch C (1964) The diagnosis of iron deficiency anemia. AM J MED 37(1):62–70. https://doi.org/10.1016/0002-9343(64)90212-8

    Article  CAS  PubMed  Google Scholar 

  36. Chen S, Wu X, Wang X, Shao Y, Tu Q, Yang H, Yin J, Yin Y (2020) Responses of intestinal microbiota and immunity to increasing dietary levels of iron using a piglet model. Front Cell Dev Biol 8:603392. https://doi.org/10.3389/fcell.2020.603392

    Article  PubMed  PubMed Central  Google Scholar 

  37. Jaeggi T, Kortman GA, Moretti D, Chassard C, Holding P, Dostal A, Boekhorst J, Timmerman HM, Swinkels DW, Tjalsma H, Njenga J, Mwangi A, Kvalsvig J, Lacroix C, Zimmermann MB (2015) Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut 64(5):731–742. https://doi.org/10.1136/gutjnl-2014-307720

    Article  CAS  PubMed  Google Scholar 

  38. Kaitha S, Bashir M, Ali T (2015) Iron deficiency anemia in inflammatory bowel disease. World J Gastrointest Pathophysiol 6(3):62–72. https://doi.org/10.4291/wjgp.v6.i3.62

    Article  PubMed  PubMed Central  Google Scholar 

  39. Saneela S, Iqbal R, Raza A, Qamar MF (2019) Hepcidin: a key regulator of iron. J Pak Med Assoc 69(8):1170–1175

    PubMed  Google Scholar 

  40. Kwiecień M, Samolińska W, Bujanowicz-haraś B (2015) Effects of iron-glycine chelate on growth, carcass characteristic, liver mineral concentrations and haematological and biochemical blood parameters in broilers. J Anim Physiol Anim Nutr (Berl) 99(6):1184–1196. https://doi.org/10.1111/jpn.12322

    Article  CAS  PubMed  Google Scholar 

  41. Kobayashi Y, Imai N, Uenishi K (2020) Attempt to determine the cut-off value of serum ferritin for iron deficiency in male college student runners. J Nutr Sci Vitaminol (Tokyo) 66(5):432–440. https://doi.org/10.3177/jnsv.66.432

    Article  CAS  PubMed  Google Scholar 

  42. Furugouri K (1972) Effect of elevated dietary levels of iron on iron store in liver, some blood constituents and phosphorus deficiency in young swine. J Anim Sci 34(4):573–577. https://doi.org/10.2527/jas1972.344573x

    Article  CAS  PubMed  Google Scholar 

  43. Wensing T, A A, S A, (1986) Some aspects of extra iron supply in veal calf fattening. Vet Res Commun 10(4):283–296. https://doi.org/10.1007/BF02213991

    Article  CAS  PubMed  Google Scholar 

  44. Lin X, Gou Z, Wang Y, Li L, Fan Q, Ding F, Zheng C, Jiang S (2020) Effects of dietary iron level on growth performance, immune organ indices and meat quality in Chinese yellow broilers. Animals (Basel) 10(4):670. https://doi.org/10.3390/ani10040670

    Article  PubMed  Google Scholar 

  45. Xie C, Elwan H, Elnesr S, Dong X, Feng J, Zou X (2019) Effects of iron glycine chelate on laying performance, antioxidant activities, serum biochemical indices, iron concentrations and transferrin mRNA expression in laying hens. J Anim Physiol Anim Nutr (Berl) 103(2):547–554. https://doi.org/10.1111/jpn.13061

    Article  CAS  PubMed  Google Scholar 

  46. Rincker M, Hill G, Link J, Rowntree J (2004) Effects of dietary iron supplementation on growth performance, hematological status, and whole-body mineral concentrations of nursery pigs. J Anim Sci 82(11):3189–3197. https://doi.org/10.2527/2004.82113189x

    Article  CAS  PubMed  Google Scholar 

  47. Knutson M (2010) Iron-sensing proteins that regulate hepcidin and enteric iron absorption. Annu Rev Nutr 30:149–171. https://doi.org/10.1146/annurev.nutr.012809.104801

    Article  CAS  PubMed  Google Scholar 

  48. Yang L, Wang H, Yang X, Wu Q, An P, Jin X, Liu W, Huang X, Li Y, Yan S, Shen S, Liang T, Min J, Wang F (2020) Auranofin mitigates systemic iron overload and induces ferroptosis via distinct mechanisms. Signal Transduct Target Ther 5(1):138. https://doi.org/10.1038/s41392-020-00253-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Li S, Lu L, Hao S, Wang Y, Zhang L, Liu S, Liu B, Li K, Luo X (2011) Dietary manganese modulates expression of the manganese-containing superoxide dismutase gene in chickens. J Nutr 141(2):189–194. https://doi.org/10.3945/jn.110.126680

    Article  CAS  PubMed  Google Scholar 

  50. Goncalves J, Moog S, Morin A, Gentric G, Müller S, Morrell AP, Kluckova K, Stewart TJ, Andoniadou CL, Lussey-Lepoutre C, Bénit P, Thakker A, Vettore L, Roberts J, Rodriguez R, Mechta-Grigoriou F, Gimenez-Roqueplo AP, Letouzé E, Tennant DA, Favier J (2021) Loss of SDHB promotes dysregulated iron homeostasis, oxidative stress, and sensitivity to ascorbate. Cancer Res 81(13):3480–3494. https://doi.org/10.1158/0008-5472.CAN-20-2936

    Article  CAS  PubMed  Google Scholar 

  51. Rao J, Jagadeesan V (1996) Lipid Peroxidation and activities of antioxidant enzymes in iron deficiency and effect of carcinogen feeding. Free Radic Biol Med 21(1):103–108. https://doi.org/10.1016/0891-5849(95)02212-0

    Article  CAS  PubMed  Google Scholar 

  52. Tavsan Z, Ayar Kayali H (2013) The Effect of iron and copper as an essential nutrient on mitochondrial electron transport system and lipid peroxidation in Trichoderma harzianum. Appl Biochem Biotechnol 170(7):1665–1675. https://doi.org/10.1007/s12010-013-0273-4

    Article  CAS  PubMed  Google Scholar 

  53. Wan J, Ren H, Wang J (2019) Iron toxicity, lipid peroxidation and ferroptosis after intracerebral haemorrhage. Stroke Vasc Neurol 4(2):93–95. https://doi.org/10.1136/svn-2018-000205

    Article  PubMed  PubMed Central  Google Scholar 

  54. Weiss Sachdev S, Sunde RA (2001) Selenium regulation of transcript abundance and translational efficiency of glutathione peroxidase-1 and -4 in rat liver. Biochem J 357(Pt 3):851–8. https://doi.org/10.1042/0264-6021:3570851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Zhang L, Lu L, Zhang L, Luo X (2016) The chemical characteristics of organic iron sources and their relative bioavailabilities for broilers fed a conventional corn-soybean meal diet. J Anim Sci 94(6):2378–2396. https://doi.org/10.2527/jas.2016-0297

    Article  CAS  PubMed  Google Scholar 

  56. Liu Y, Beyer A, Aebersold R (2016) On the dependency of cellular protein levels on mRNA abundance. Cell 165(3):535–550. https://doi.org/10.1016/j.cell.2016.03.014

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was funded by the business fund of Beijing Academy of Agriculture and Forestry Science (under Grant number: XMSSYJJ2021) and national modern agricultural science and technology city industry cultivation and achievements benefiting the people project of Beijing Municipal Commission of Science and Technology (number: Z171100001517003).

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  1. Zheng Wang and Dongdong Zhao have contributed equally to this work.

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 & Yuxin Shao

  2. Faculty of Animal Science and Technology, Gansu Agricultural University, No. 1 Yingmen Village, Anning District, Lanzhou, 730070, Gansu Province, China

    Dongdong Zhao, Shizhen Qin, Zhaoguo Shi & Yangyang Wang

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  1. Zheng Wang
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Contributions

Dongdong Zhao carried out the experiments. Shizhen Qin, Zhaoguo Shi, Xing Li, and Yangyang Wang processed the data. Zheng Wang and Yuxin Shao designed the experiment and wrote the paper. The final manuscript was read and approved by all authors.

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Correspondence to Yuxin Shao.

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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.

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Wang, Z., Zhao, D., Qin, S. et al. Effects of Dietary Supplementation with Iron in Breeding Pigeons on the Blood Iron Status, Tissue Iron Content, and Full Expression of Iron-Containing Enzymes of Squabs. Biol Trace Elem Res 201, 4538–4546 (2023). https://doi.org/10.1007/s12011-022-03530-x

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