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Dietary Copper Supplementation Increases Growth Performance by Increasing Feed Intake, Digestibility, and Antioxidant Activity in Rex Rabbits

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Abstract

Copper is often used as a growth promoter, at the same time copper is one of the most important essential trace elements for fur animals, especially Rex rabbits. However, too much copper added to the diet may harm animal health, and copper excreted in feces can pollute the environment. In this study, 3-month-old Rex rabbits were randomly divided into four groups and fed a basal diet containing 0, 30, 60, or 120 mg/kg Cu for 5 weeks. The diet supplemented with 30 mg/kg Cu significantly increased (P < 0.05) the average daily feed intake (ADFI) and the average daily gain (ADG) and also the activity of serum Cu–Zn (zinc) superoxide dismutase and the digestibility of ether extract. Supplemental Cu up to 120 mg/kg did not significantly adversely affect the Zn metabolism of growing Rex rabbits. Overall, the data in this study indicate that 30 mg/kg is the optimal level of Cu supplementation in the diet of growing Rex rabbits. The results will provide a reference to improve the breeding of Rex rabbits and possibly other animals. In follow-up studies, the amount of copper in the diet should be reduced as much as possible from the baseline of 30 mg/kg copper.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Abbo el-Ezz ZR, Salem MH, Sassan GA, El-komy AG, Abd EI Moula (1996) Effect of different levels of copper sulfate supplementation on some physical traits of rabbits. In: Lebas F (ed) Proceedings of the 6th World Rabbit Congress, Toulouse. Association Francaise de Cuniculture, Lempdes, pp 59–64

  2. Harris ED (2003) Basic and clinical aspects of copper. Crit Rev Clin Lab Sci 40(5):547–586. https://doi.org/10.1080/10408360390250649

    Article  CAS  PubMed  Google Scholar 

  3. Turski ML, Thiele DJ (2009) New roles for copper metabolism in cell proliferation, signaling, and disease. J Biol Chem 284(2):712–721. https://doi.org/10.1074/jbc.R800055200

    Article  Google Scholar 

  4. Pang Y, Patterson JA, Applegate TJ (2009) The influence of copper concentration and source on ileal microbiota. Poult Sci 88(3):586–592. https://doi.org/10.3382/ps.2008-00243

    Article  CAS  PubMed  Google Scholar 

  5. Omole OA, Onawunmi (1979) Effect of copper on growth and serum constituents of immunized and non-immunized rabbits infected with Trypanosoma brucei. Ann Parasitol Hum Comp 54(5):495–506. https://doi.org/10.1051/parasite/1979545495

    Article  CAS  PubMed  Google Scholar 

  6. Skrivanová V, Skrivan M, Marounek M, Baran M (2001) Effect of feeding supplemental copper on performance, fatty acid profile and on cholesterol contents and oxidative stability of meat of rabbits. Arch Tierernahr 54(4):329–339. https://doi.org/10.1080/17450390109381989

    Article  PubMed  Google Scholar 

  7. Wang JG, Zhu XY, Guo YZ, Wang Z, Zhao BY, Yin YH, Liu GW (2015) Influence of dietary copper on serum growth-related hormone levels and growth performance of weanling pigs. Biol Trace Elem Res 172(1):134–139. https://doi.org/10.1007/s12011-015-0574-2

    Article  CAS  PubMed  Google Scholar 

  8. Coble KF, Derouchey JM, Tokach MD, Dritz SS, Usry JL (2017) The effects of copper source and concentration on growth performance, carcass characteristics, and pen cleanliness in finishing pigs. J Anim Sci 95(9):4052–4059. https://doi.org/10.2527/jas2017.1624

    Article  CAS  PubMed  Google Scholar 

  9. Rochell SJ, Usry JL, Parr TM, Parsons CM, Dilger RN (2017) Effects of dietary copper and amino acid density on growth performance, apparent metabolizable energy, and nutrient digestibility in Eimeria acervulina-challenged broilers. Poult Sci 96(3):602–610. https://doi.org/10.3382/ps/pew276

    Article  CAS  PubMed  Google Scholar 

  10. Hedemann MS, Jensen BB, Poulsen HD (2016) Influence of dietary zinc and copper on digestive enzyme activity and intestinal morphology in weaned pigs. J Anim Sci 84(12):3310–3320. https://doi.org/10.2527/jas.2005-701

    Article  CAS  Google Scholar 

  11. Cavalcante SG, Ferreira WM, Valente SS, Santiago GS, Dias JCCA, Naranjo AP (2002) Copper bioavailability from different sources for rabbits. Arq Bras Med Vet Zoo 54:290–294. https://doi.org/10.1590/S0102-09352002000300012

    Article  Google Scholar 

  12. Julian W, Carlos DB (2015) Mineral needs of rabbits. In: Guo YL, Qiu LW, Zhou XY (eds) Nutrition of The Rabbit, vol 7, 2nd edn. China Agricultural Publishing House, Bei Jing, China, pp 186–189

    Google Scholar 

  13. Kumar V, Kalita J, Bora HK (2016) Misra UK (2016) relationship of antioxidant and oxidative stress markers in different organs following copper toxicity in a rat model. Toxicol Appl Pharw 293:37–43. https://doi.org/10.1016/j.taap.2016.01.007

    Article  CAS  Google Scholar 

  14. Liu L, Zeng D, Yang M, Wen B, Lai J, Zhou Y, Sun H, Xiong LC, Wang J, Lin YC, Pan KC, Jing B, Wang P, Ni XQ (2018) Probiotic Clostridium butyricum improves the growth performance, immune function, and gut microbiota of weaning rex rabbits. Probiotics Antimicro 11:1278–1292. https://doi.org/10.1007/s12602-018-9476-x

    Article  CAS  Google Scholar 

  15. Antonella DZ, Zsolt S (2011) The role of rabbit meat as functional food. Meat Sci 88(3):319–331. https://doi.org/10.1016/j.meatsci.2011.02.017

    Article  CAS  Google Scholar 

  16. Liu Z, Wu X, Zhang T, Guo J, Gao XY, Yang FH, Xing XM (2015) Effects of dietary copper and zinc supplementation on growth performance, tissue mineral retention, antioxidant status, and fur quality in growing-furring blue foxes (Alopex lagopus). Biol Trace Elem Res 168(2):401–410. https://doi.org/10.1007/s12011-015-0376-6

    Article  CAS  PubMed  Google Scholar 

  17. Wu XZ, Liu Z, Guo JG, Wan CM, Zhang TT, Cui H, Yang FH, Gao XH (2015) Influence of dietary zinc and copper on apparent mineral retention and serum biochemical indicators in young male mink (mustela vison). Biol Trace Elem Res 165(1):59–66. https://doi.org/10.1007/s12011-014-0220-4

    Article  CAS  PubMed  Google Scholar 

  18. NRC (1977) Nutrient Requirements of Rabbit. National Academies Press, Washington

    Google Scholar 

  19. Schlolaut W (1987) Nutritional needs and feeding of German angora rabbits. J Appl Rabbit Res 10:111–121

    Google Scholar 

  20. Zhang YC, Wang EN, Li YW, Wang YX, Cheng GM, LIU JS, Jiang BY (2019) Effects of dietary copper supplementation level on growth performance, wool performance, serum biochemical indices and copper-containing enzyme activities and visceral organ development of 2-to 4-month-old long hairy rabbits. Chin J Anim Nutr 31(10):4622–4629. https://doi.org/10.3969/j.issn.1006-267x.2019.10.026

    Article  Google Scholar 

  21. Chen XY, Yang GY, Zhang B, Li F, Liu L, Li FC (2020) Effects of manganese-supplemented diets on growth performance, blood biochemistry, nitrogen metabolism and skeletal development of Rex rabbits. J Trace Elem Med Biol 61:126543. https://doi.org/10.1016/j.jtemb.2020.126543

    Article  CAS  PubMed  Google Scholar 

  22. Blasco A, Ouhayoun J, Masoero G (1993) Harmonization of criteria and terminology in rabbit meat research. World Rabbit Sci 1:3–10. https://doi.org/10.4995/wrs.1993.189

    Article  Google Scholar 

  23. AOAC (2000) Official methods of analysis of AOAC International, 17th edn. Association Office Analysis Chemistry, Gaithersburg

    Google Scholar 

  24. Hu XY, Wang YF, Sheikhahmadi A, Li XL, Buyse J, Lin H, Song ZG (2019) Effects of dietary energy level on appetite and central AMPK in broilers. J Anim Sci 97(11):4488–4495. https://doi.org/10.1093/jas/skz312

    Article  PubMed  PubMed Central  Google Scholar 

  25. Liu L, Sui XY, Li FC (2017) Effect of dietary copper addition on lipid metabolism in rabbits. Food Nutr Res 61(1):1348866. https://doi.org/10.1080/16546628.2017.1348866

    Article  CAS  Google Scholar 

  26. Livak KJ, Schmittgen TD (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 

  27. Ayyat MS, Marai IFM, Alazab AM (1995) Copper protein nutrition of New Zealand white rabbits under Egyptian conditions. World Rabbit Sci 3:113–118. https://doi.org/10.4995/wrs.1995.249

    Article  Google Scholar 

  28. Bassuny SM (1991) The effect of copper sulfate supplement on rabbit performance under Egyptian conditions. J Appl Rabbit Res 14:93–97

    Google Scholar 

  29. Brandão-Neto J, Vieira JG, Nonaka KO, Marchini JS, Antunes-Rodrigues J (1988) Effect of copper on the secretion of human growth hormone. Braz J Med Biol Anim Sci 21:259–261

    Google Scholar 

  30. Krishnamoorthy L, Cotruvo JA, Chan J, Kaluarachchi H, Muchenditsi A, Pendyala VS, Jia S, Aron AT, Ackerman CM, Wal MNV, Guan T, Smaga LP, Farhi SL, New EJ, Lutsenko S, Chang CJ (2016) Copper regulates cyclic-AMP-dependent lipolysis. Nat Chem Biol 12(8):586–592. https://doi.org/10.1038/nchembio.2098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Carpenter CB, Woodworth JC, Derouchey JM, Tokach MD, Goodband RD, Dritz SS, Wu FZ, Rambo ZJ (2019) Effects of increasing copper from either copper sulfate or combinations of copper sulfate and a copper–amino acid complex on finishing pig growth performance and carcass characteristics. Transl Anim Sci 3:1263–1269. https://doi.org/10.1093/tas/txz112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Dove CR (1995) The effect of copper level on nutrient utilization of weanling pigs. J Anim Sci 73(1):166–171. https://doi.org/10.2527/1995.731166x

    Article  CAS  PubMed  Google Scholar 

  33. Sugawara N, Li D, Sugawara C, Miyake H (1995) Response of hepatic function to hepatic copper deposition in rats fed a diet containing copper. Biol Trace Elem Res 49(2/3):161–169. https://doi.org/10.1007/BF02788965

    Article  CAS  PubMed  Google Scholar 

  34. Hwang DF, Wang LC, Cheng HM (1998) Effect of taurine on toxicity of copper in rats. Food Chem Toxicol 36:239–244. https://doi.org/10.1016/s0278-6915(97)00146-4

    Article  CAS  PubMed  Google Scholar 

  35. Mao WL, Sun QQ, Fan J, Lin S, Ye B (2016) AST to platelet ratio index predicts mortality in hospitalized patients with hepatitis B-related decompensated cirrhosis. Medicine 95(9):e2946. https://doi.org/10.1097/MD.0000000000002946

    Article  PubMed  PubMed Central  Google Scholar 

  36. Roberts EA, Sarkar B (2008) Liver as a key organ in the supply, storage, and excretion of copper. Am J Clin Nutr 88(3):851S–854S. https://doi.org/10.1093/ajcn/88.3.851S

    Article  CAS  PubMed  Google Scholar 

  37. Fu JG, Gao YX, Li Y, Li QF, Cao YF, Zhang XJ, Li JG (2020) Effects of copper on lactation, the expression of copper metabolic protein and enzyme-related genes in the liver of Chinese Holstein dairy cows. Chin J Vet Sci 40(1):162–178. https://doi.org/10.16303/j.cnki.1005-4545.2020.01.27

    Article  CAS  Google Scholar 

  38. Zhang F, Zheng WJ, Yao W (2020) Effects of dietary copper level on the tissue morphology, copper metabolism and redox balance of intestines and liver in SD rats. J Nanjing Agric Univ 43(4):728–739. https://doi.org/10.7685/jnau.201907029

    Article  Google Scholar 

  39. Zhong W, Liu H, Luo G, Chang Z, Li G (2014) Dietary copper supplementation improves pelt characteristics of female silver fox (Vulpes fulva) during the winter fur-growing season. J Anim Sci 85(7):757–762. https://doi.org/10.1111/asj.12208

    Article  CAS  Google Scholar 

  40. Sternlieb I (1980) Copper and the liver. Gastroenterology 78(6):1615–1628

    Article  CAS  PubMed  Google Scholar 

  41. Sato M, Gitlin JD (1991) Mechanisms of copper incorporation during the biosynthesis of human ceruloplasmin. J Biol Chem 266(8):5128–5134

    Article  CAS  PubMed  Google Scholar 

  42. Terada K, Kawarada Y, Miura N, Yasui O, Koyama K, Sugiyama T (1995) Copper incorporation into ceruloplasmin in rat livers. Bba-Bioenergetics 1270(1):58–62. https://doi.org/10.1016/0925-4439(94)00072-x

    Article  PubMed  Google Scholar 

  43. Jarosz LS, Marek A, Gradzki Z, Kwiecień M, Kaczmarek B (2017) The effect of feed supplementation with a copper-glycine chelate and copper sulphate on selected humoral and cell-mediated immune parameters, plasma superoxide dismutase activity, ceruloplasmin and cytokine concentration in broiler chickens. J Anim Physiol Anim Nutr 102(1):e326–e336. https://doi.org/10.1111/jpn.12750

    Article  CAS  Google Scholar 

  44. Bremner I (1987) Involvement of metallothionein in the hepatic metabolism of copper. J Nutr 117(1):19–29. https://doi.org/10.1093/jn/117.1.19

    Article  CAS  PubMed  Google Scholar 

  45. Valentine JS, Gralla EB (1997) Delivering copper inside yeast and human cells. Science 278(5339):817–818. https://doi.org/10.1126/science.278.5339.817

    Article  CAS  PubMed  Google Scholar 

  46. Kimura T, Nishioka H (1997) Intracellular generation of superoxide by copper sulphate in Escherichia coli. Mutat Res-Gen Tox En 389(2/3):237–242. https://doi.org/10.1016/s1383-5718(96)00153-2

    Article  CAS  Google Scholar 

  47. Ruth D, Magdalena A, Brenda H, Carl K, Marc S, Dennis T, Mcardle Harry T (2007) How reliable and robust are current biomarkers for copper status? Br J Nutr 98(4):676–683. https://doi.org/10.1017/S0007114507798951

    Article  CAS  Google Scholar 

  48. Turnlund JR, Keyes WR, Peiffer GL, Scott KC (1998) Copper absorption, excretion, and retention by young men consuming low dietary copper determined by using the stable isotope 65cu. Am J Clin Nutr 67(6):1219–1225. https://doi.org/10.1093/ajcn/67.6.1219

    Article  CAS  PubMed  Google Scholar 

  49. Bradley BD, Graber G, Condon RJ, Frobish LT (1983) Effects of graded levels of dietary copper on copper and iron concentrations in swine tissues. J Anim Sci 56(3):625–630. https://doi.org/10.2527/jas1983.563625x

    Article  CAS  PubMed  Google Scholar 

  50. Zhang SSZ, Noordin MM, Rahman SOA, Haron J (2000) Effects of copper overload on hepatic lipid peroxidation and antioxidant defense in rats. Vet Hum Toxicol 42(5):261–264

    CAS  PubMed  Google Scholar 

  51. Chowdhury SD, Paik IK, Namkung H, Lim HS (2004) Responses of broiler chickens to organic copper fed in the form of copper–methionine chelate. Anim Feed Sci Technol 115(3–4):281–293. https://doi.org/10.1016/j.anifeedsci.2004.03.009

    Article  CAS  Google Scholar 

  52. Valenzuela C, Daniel Lopez de Romaña Schmiede C, María Sol Morales Olivares M, Pizarro F (2011) Total iron, heme iron, zinc, and copper content in rabbit meat and viscera. Biol Trace Elem Res 143(3):1489–1496. https://doi.org/10.1007/s12011-011-8989-x

    Article  CAS  PubMed  Google Scholar 

  53. Feng XD, Deng JG, Wang W, Guo XN, Wang X, Wu ZM, Zhang YZ (2009) Changes of contents of copper and zinc in tissues and manure of pigs fed with high-level copper and zinc diets. Journal of Inspection and Quarantine 019(001):21–23

    Google Scholar 

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Funding

This research was funded by the Natural Science Foundation of Shandong Province (ZR2018MC025), the Modern Agri-industry Technology Research System (CARS-43-B-1), and the Shandong “Double Tops” Program.

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Correspondence to Li Fuchang.

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Li, F., Liu, L., Chen, X. et al. Dietary Copper Supplementation Increases Growth Performance by Increasing Feed Intake, Digestibility, and Antioxidant Activity in Rex Rabbits. Biol Trace Elem Res 199, 4614–4623 (2021). https://doi.org/10.1007/s12011-020-02568-z

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