Skip to main content
SpringerLink
Log in

Effects of Inorganic and Organic Manganese Supplementation on Growth Performance, Tibia Development, and Oxidative Stress in Broiler Chickens

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Manganese (Mn) is an essential trace element for broiler chickens; its deficiency causes tibial dyschondroplasia (TD) characterized by lameness and growth retardation. Inorganic and organic manganese sources are used in global poultry production, but there is a lack of systematic investigations to compare the bioavailability among them. In this study, 120 1-day-old Arbor Acres (AA) broilers were randomly divided into four groups (n = 30), i.e., control group (Mn sulfate, 60 mg/kg), Mn-D group (Mn deficiency, 22 mg/kg), Mn-Gly group (Mn glycinate, 60 mg/kg), and Mn-Pro group (Mn proteinate, 60 mg/kg). During the 42-day experiment, growth performance, tibial bone parameters, pathological index changes, serum biochemical changes, and oxidative stress indicators were evaluated. These results not only suggested that Mn plays a crucial role in the normal development of tibia and the maintenance of redox homeostasis in broilers, but also proved that organic Mn supplementation, especially Mn proteinate, improved the tibia development and the absorption efficiency, as well as overall oxidative stress status of broilers, suggesting that it had greater bioavailability than inorganic Mn. Thus, application of organic Mn source may be an effective way to reduce economic losses and resolve animal welfare concerns due to TD in commercial poultry farming.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

The datasets generated used to support the findings of the current study are available from the corresponding author on reasonable request.

Code Availability

Not applicable.

Abbreviations

TD:

Tibial dyschondroplasia

ECM:

Extracellular matrix

GP:

Growth plate

AA:

Arbor Acres

FCR:

Feed conversion ratio

ADG:

Average dairy gain

ADFI:

Average daily feed intake

AKP:

Alkaline phosphatase

Nrf2:

Nuclear factor erythroid-2 related factor 2

MnSOD:

Manganese superoxide dismutase

GPx:

Glutathione peroxidase

NQO1:

NADH quinone oxidoreductase 1

HO-1:

Heme oxygenase-1

References

  1. Yang T, Wang X, Wen M, Zhao H, Liu G, Chen X, Tian G, Cai J, Jia G (2021) Effect of manganese supplementation on the carcass traits, meat quality, intramuscular fat, and tissue manganese accumulation of Pekin duck. Poult Sci 100(5):101064–101075

  2. Pedersen IJ, Tahamtani FM, Forkman B, Young JF, Poulsen HD, Riber AB (2020) Effects of environmental enrichment on health and bone characteristics of fast growing broiler chickens. Poult Sci 99(4):1946–1955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Steven D, BainWatkins BA (1993) Local modulation of skeletal growth and bone modeling in poultry. Am Inst Nutr 0022–3166:317–322

    Google Scholar 

  4. Van Wyhe RC, Applegate TJ, Lilburn MS, Karcher DM (2012) A comparison of long bone development in historical and contemporary ducks. Poult Sci 91(11):2858–2865

    Article  PubMed  Google Scholar 

  5. Amend SR, Valkenburg KC, Pienta KJ (2016) Murine hind limb long bone dissection and bone marrow isolation. J Vis Exp (110):53936

  6. Waqas M, Qamar H, Zhang J, Yao W, Li A, Wang Y, Iqbal M, Mehmood K, Jiang X, Li J (2020) Puerarin enhance vascular proliferation and halt apoptosis in thiram-induced avian tibial dyschondroplasia by regulating HIF-1alpha, TIMP-3 and BCL-2 expressions. Ecotoxicol Environ Saf 190:110126

    Article  CAS  PubMed  Google Scholar 

  7. Mehmood K, Zhang H, Iqbal MK, Rehman MU, Shahzad M, Li K, Huang S, Nabi F, Zhang L, Li J (2017) In vitro effect of apigenin and danshen in tibial dyschondroplasia through inhibition of heat-shock protein 90 and vascular endothelial growth factor expressions in avian growth plate cells. Avian Dis 61(3):372–377

    Article  PubMed  Google Scholar 

  8. Zhang H, Mehmood K, Jiang X, Li Z, Yao W, Zhang J, Tong X, Wang Y, Li A, Waqas M et al (2019) Identification of differentially expressed MiRNAs profile in a thiram-induced tibial dyschondroplasia. Ecotoxicol Environ Saf 175:83–89

    Article  CAS  PubMed  Google Scholar 

  9. Zhang H, Mehmood K, Jiang X, Yao W, Iqbal M, Li K, Tong X, Wang L, Wang M, Zhang L et al (2018) Effect of icariin on tibial dyschondroplasia incidence and tibial characteristics by regulating P2RX7 in chickens. Biomed Res Int 2018:6796271

    PubMed  PubMed Central  Google Scholar 

  10. Klimis-Tavantzis DJ, Kris-Ethertion PM, Leach RM Jr (1983) The effect of dietary manganese deficiency on cholesterol and lipid metabolism in the estrogentreated chicken and the laying hen. American Institute of Nutrition 113:320–327

    CAS  Google Scholar 

  11. Ahola JK, Baker DS, Burns PD, Mortimer RG, Enns RM, Whittier JC, Geary TW, Engle TE (2004) Effect of copper, zinc, and manganese supplementation and source on reproduction, mineral status, and performance in grazing beef cattle over a two-year period. J Anim Sci 82:2375–2383

    Article  CAS  PubMed  Google Scholar 

  12. Wu C, Yuan G, Mo R, Huang Y, Luo T, Wang J (2019) Effect of endoplasmic reticulum stress involved in manganeseinduced neurotoxicity in rats. Mol Med Rep 19(6):5169–5176

    CAS  PubMed  Google Scholar 

  13. Asling CW, Hurley LS (1963) The influence of trace elements on the skeleton. Clin Orthop Relat Res 27:213–264

    CAS  PubMed  Google Scholar 

  14. Hurley LS, Gowan J, Milhaud G (1969) Calcium metabolism in manganese-deficient and zinc-deficient rats. Proc Soc Exp Biol Med 130(3):856–860

    Article  CAS  PubMed  Google Scholar 

  15. Wang J, Wang ZY, Wang ZJ, Liu R, Liu SQ, Wang L (2015) Effects of manganese deficiency on chondrocyte development in tibia growth plate of Arbor Acres chicks. J Bone Miner Metab 33(1):23–29

    Article  PubMed  CAS  Google Scholar 

  16. Cashman K, Flynn A (1998) Trace elements and bone metabolism. Bibl Nutr Dieta 54:150–164

    CAS  Google Scholar 

  17. Zofkova I, Nemcikova P, Matucha P (2013) Trace elements and bone health. Clin Chem Lab Med 51(8):1555–1561

    Article  CAS  PubMed  Google Scholar 

  18. Shao Y, Sun G, Cao S, Lu L, Zhang L, Liao X, Luo X (2019) Bone phosphorus retention and bone development of broilers at different ages. Poult Sci 98(5):2114–2121

    Article  CAS  PubMed  Google Scholar 

  19. Rath NC, Huff GR, Huff WE, Balog JM (2000) Factors regulating bone maturity and strength in poultry. Poult Sci 79(7):1024–1032

    Article  CAS  PubMed  Google Scholar 

  20. Jahejo AR, Tian WX (2021) Cellular, molecular and genetical overview of avian tibial dyschondroplasia. Res Vet Sci 135:569–579

    Article  CAS  PubMed  Google Scholar 

  21. Gerber HP, Ferrara N (2000) Angiogenesis and bone growth. Trends Cardiovasc Med 10(5):223–228

    Article  CAS  PubMed  Google Scholar 

  22. Mehmood K, Zhang H, Yao W, Jiang X, Waqas M, Li A, Wang Y, Lei L, Zhang L, Qamar H et al (2019) Protective effect of astragaloside IV to inhibit thiram-induced tibial dyschondroplasia. Environ Sci Pollut Res Int 26(16):16210–16219

    Article  CAS  PubMed  Google Scholar 

  23. Zhang H, Mehmood K, Jiang X, Yao W, Iqbal M, Waqas M, Rehman MU, Li A, Shen Y, Li J (2018) Effect of tetramethyl thiuram disulfide (thiram) in relation to tibial dyschondroplasia in chickens. Environ Sci Pollut Res Int 25(28):28264–28274

    Article  CAS  PubMed  Google Scholar 

  24. Wang F, Lu L, Li S, Liu S, Zhang L, Yao J, Luo X (2012) Relative bioavailability of manganese proteinate for broilers fed a conventional corn-soybean meal diet. Biol Trace Elem Res 146(2):181–186

    Article  CAS  PubMed  Google Scholar 

  25. Henry PR, Ammerman CB, Miles RD (1989) Relative bioavailability of manganese in a manganese-methionine complex for broiler chicks. Poult Sci 68(1):107–112

    Article  CAS  PubMed  Google Scholar 

  26. Henry PR, Ammerman CB, Littell RC (1992) Relative bioavailability of manganese from a manganese-methionine complex and inorganic sources for ruminants. J Dairy Sci 75(12):3473–3478

    Article  CAS  PubMed  Google Scholar 

  27. Baker DH, Halpin KM (1987) Efficacy of a manganese-protein chelate compared with that of manganese sulfate for chicks. Poult Sci 66(9):1561–1563

    Article  CAS  PubMed  Google Scholar 

  28. Scheideler SE (1991) Interaction of dietary calcium, manganese, and manganese source (Mn oxide or Mn methionine complex) on chick performance and manganese utilization. Biol Trace Elem Res 29(3):217–228

    Article  CAS  PubMed  Google Scholar 

  29. Crenshaw TD, Peo ER Jr, Lewis AJ, Moser BD (1981) Bone strength as a trait for assessing mineralization in swine: a critical review of techniques involved. J Anim Sci 53:827–835

    Article  Google Scholar 

  30. Gong Z-G, Wang X-Y, Wang J-H, Fan R-F, Wang L (2019) Trehalose prevents cadmium-induced hepatotoxicity by blocking Nrf2 pathway, restoring autophagy and inhibiting apoptosis. J Inorg Biochem 192:62–71

    Article  CAS  PubMed  Google Scholar 

  31. Wang Y, Jiang L, Li Y, Luo X, He J (2016) Effect of different selenium supplementation levels on oxidative stress, cytokines, and immunotoxicity in chicken thymus. Biol Trace Elem Res 172(2):488–495

    Article  CAS  PubMed  Google Scholar 

  32. Luan H, Wang Y, Li Y, Cui Z, Chang S, Zhao P (2016) Development of a real-time quantitative RT-PCR to detect REV contamination in live vaccine. Poult Sci 95(9):2023–2029

    Article  CAS  PubMed  Google Scholar 

  33. Noetzold TL, Vieira SL, Favero A, Horn RM, Silva CM, Martins GB (2020) Manganese requirements of broiler breeder hens. Poult Sci 99(11):5814–5826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mwangi S, Timmons J, Ao T, Paul M, Macalintal L, Pescatore A, Cantor A, Dawson KA (2019) Effect of manganese preconditioning and replacing inorganic manganese with organic manganese on performance of male broiler chicks. Poult Sci 98(5):2105–2113

    Article  CAS  PubMed  Google Scholar 

  35. Li J, Bi D, Pan S, Zhang Y, Zhou D (2008) Effects of high dietary vitamin A supplementation on tibial dyschondroplasia, skin pigmentation and growth performance in avian broilers. Res Vet Sci 84(3):409–412

    Article  CAS  PubMed  Google Scholar 

  36. Farquharson C, Jefferies D (2000) Chondrocytes and longitudinal bone growth: the development of tibial dyschondroplasia. Poult Sci 79(7):994–1004

    Article  CAS  PubMed  Google Scholar 

  37. Liu R, Jin C, Wang Z, Wang Z, Wang J, Wang L (2015) Effects of manganese deficiency on the microstructure of proximal tibia and OPG/RANKL gene expression in chicks. Vet Res Commun 39(1):31–37

    Article  PubMed  Google Scholar 

  38. Yang G, Tian X, Dong S, Peng M, Wang D (2015) Effects of dietary Bacillus cereus G19, B. cereus BC-01, and Paracoccus marcusii DB11 supplementation on the growth, immune response, and expression of immune-related genes in coelomocytes and intestine of the sea cucumber (Apostichopus japonicus Selenka). Fish Shellfish Immunol 45(2):800–807

    Article  CAS  PubMed  Google Scholar 

  39. Deng L, Liu D, Zhang Q, Luo J, Zhong G (2020) Effect of the mixture of mulberry leaf powder and KGM flour on promoting calcium absorption and bone mineral density in vivo. J Sci Food Agric 100(9):3587–3597

    Article  CAS  PubMed  Google Scholar 

  40. Wang CY, Xia WH, Wang L, Wang ZY (2021) Manganese deficiency induces avian tibial dyschondroplasia by inhibiting chondrocyte proliferation and differentiation. Res Vet Sci 140:164–170

    Article  CAS  PubMed  Google Scholar 

  41. Zhang H, Mehmood K, Li K, Rehman MU, Jiang X, Huang S, Wang L, Zhang L, Tong X, Nabi F et al (2018) Icariin ameliorate thiram-induced tibial dyschondroplasia via regulation of WNT4 and VEGF expression in broiler chickens. Front Pharmacol 9:123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Berta E, Andrásofszky E, Bersényi A, Glávits R, Gáspárdy A, Fekete SG (2004) Effect of inorganic and organic manganese supplementation on the performance and tissue manganese content of broiler chicks. Acta Vet Hung 52(2):199–209

    Article  CAS  PubMed  Google Scholar 

  43. Li S, Luo X, Liu B, Crenshaw TD, Kuang X, Shao G, Yu S (2004) Use of chemical characteristics to predict the relative bioavailability of supplemental organic manganese sources for broilers. J Anim Sci 82(8):2352–2363

    Article  CAS  PubMed  Google Scholar 

  44. Li SF, Luo XG, Lu L, Liu B, Kuang X, Shao GZ, Yu SX (2008) Effect of intravenously injected manganese on the gene expression of manganese-containing superoxide dismutase in broilers. Poult Sci 87(11):2259–2265

    Article  CAS  PubMed  Google Scholar 

  45. Luo XG, Li SF, Lu L, Liu B, Kuang X, Shao GZ, Yu SX (2007) Gene expression of manganese-containing superoxide dismutase as a biomarker of manganese bioavailability for manganese sources in broilers. Poult Sci 86(5):888–894

    Article  CAS  PubMed  Google Scholar 

  46. Yu ZM, Wan XM, Xiao M, Zheng C, Zhou XL (2021) Puerarin induces Nrf2 as a cytoprotective mechanism to prevent cadmium-induced autophagy inhibition and NLRP3 inflammasome activation in AML12 hepatic cells. J Inorg Biochem 217:111389

    Article  CAS  PubMed  Google Scholar 

  47. Jiang WD, Tang RJ, Liu Y, Wu P, Kuang SY, Jiang J, Tang L, Tang WN, Zhang YA, Zhou XQ et al (2017) Impairment of gill structural integrity by manganese deficiency or excess related to induction of oxidative damage, apoptosis and dysfunction of the physical barrier as regulated by NF-kappaB, caspase and Nrf2 signaling in fish. Fish Shellfish Immunol 70:280–292

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Professor Rui-Feng Fan for his helpful advice.

Funding

This work was supported by grants from the National Natural Science Foundation of China (32072927), Shandong Provincial Natural Science Foundation of China (No. ZR2019MC068), and Youth Innovation and Technology Program in Colleges and Universities of Shandong Province (No. 2020KJF009).

Author information

Authors and Affiliations

  1. College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City, 271018, China

    Wei-Hao Xia, Liang Tang, Zhen-Yong Wang & Lin Wang

  2. Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural University, Tai’an City, 271018, China

    Wei-Hao Xia, Liang Tang, Zhen-Yong Wang & Lin Wang

  3. Shandong Provincial Engineering Technology Research Center of Animal Disease Control and Prevention, Shandong Agricultural University, Tai’an City, 271018, China

    Zhen-Yong Wang & Lin Wang

Authors
  1. Wei-Hao Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liang Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhen-Yong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Wei-hao Xia and Liang Tang: investigation, data analysis, writing the original draft and editing. Lin Wang and Zhen-Yong Wang: supervision, resources, writing review and editing, project administration, funding acquisition. All the authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Zhen-Yong Wang or Lin Wang.

Ethics declarations

Ethics Approval

All the methods and procedures were approved by Institutional Animal Care and Use committee of Shangdong Agricultural University (Approval No. 2020–04), Shandong, China.

Consent for Publication

Manuscript is approved by all the authors for publication.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xia, WH., Tang, L., Wang, ZY. et al. Effects of Inorganic and Organic Manganese Supplementation on Growth Performance, Tibia Development, and Oxidative Stress in Broiler Chickens. Biol Trace Elem Res 200, 4453–4464 (2022). https://doi.org/10.1007/s12011-021-03041-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-021-03041-1

Keywords

Search

Navigation