Meta-analysis of the effect of dietary inclusion of copper on production performance in swine

Victoria Tufiño-Loza, Renan Mena-Pérez, Diego Rodriguez-Saldaña, Jimmy Rolando Quisirumbay

Abstract


Background. Copper is a trace element that is involved in various metabolic reactions (cellular respiration, hemoglobin formation and the development of connective tissue), acting with bacteriostatic and bactericidal properties. It can be toxic and excessively excreted into the environment when used at high doses. There are many studies with different levels of inclusion and times of dietary copper supplementation with variable results, generating uncertainty among nutritionists. Objective. To measure the effect of dietary copper inclusion on productive performance in pigs through the use of meta-analysis. Methodology. 24 analyzes were run from 28 scientific articles that included a total of 3908 animals. Under the random effects model, effect size, heterogeneity, meta-regressions and publication bias were determined. Results. The results showed that copper supplementation improved average daily weight gain (+30.61 g/day, p<0.00001), average daily feed intake (+18.726 g/day, p=0.0001), feed conversion (-0.10009 kg/kg, p=0.00003) and feed efficiency (+0.00597 kg/kg, p=0.0052). High values of heterogeneity (>80%) were found in most of the variables evaluated, so meta-regressions were performed with the moderators: duration and level of supplementation, dietary level of crude protein, zinc, vitamins A and E, and number of repetitions. Implications: Optimizing rations with these data maximizes swine performance and mitigates the environmental impact of copper excretion. Conclusion. It was concluded that dietary copper supplementation improved productive performance in pigs and these results are affected by other dietary nutrients.

Keywords


nutrition; piglets; fattening; minerals; environment

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References


Aaron, D.K. and Hays, V.W., 2004. How many pigs? Statistical power considerations in swine nutrition experiments. Journal of Animal Science, 82(13_suppl), pp. E245–E254. https://doi.org/10.2527/2004.8213_supplE245x

Ayuso, M., Óvilo, C., Fernández, A., Nuñez, Y., Isabel, B., Daza, A., López-Bote, C.J. and Rey, A.I., 2015. Effects of dietary vitamin A supplementation or restriction and its timing on retinol and ?-tocopherol accumulation and gene expression in heavy pigs. Animal Feed Science and Technology, 202, pp. 62–74. https://doi.org/10.1016/j.anifeedsci.2015.01.014

Bax, L., 2016. MIX 2.0 - Professional software for meta-analysis in Excel. [Software].

Blavi, L., Solà, D., Monteiro, A., Pérez, J.F. and Stein, H.H., 2021. Inclusion of dicopper oxide instead of copper sulfate in diets for growing–finishing pigs results in greater final body weight and bone mineralization, but reduced accumulation of copper in the liver. Journal of Animal Science, 99(6), skab127. https://doi.org/10.1093/jas/skab127

Burrough, E.R., De Mille, C. and Gabler, N.K., 2019. Zinc overload in weaned pigs: tissue accumulation, pathology, and growth impacts. Journal of Veterinary Diagnostic Investigation, 31(4), pp. 537–545. https://doi.org/10.1177/1040638719852144

Canibe, N., Højberg, O., Kongsted, H., Vodolazska, D., Lauridsen, C., Nielsen, T.S. and Schönherz, A.A., 2022. Review on Preventive Measures to Reduce Post-Weaning Diarrhoea in Piglets. Animals, 12(19), 2585. https://doi.org/10.3390/ani12192585

Cao, S., Hou, L., Sun, L., Gao, J., Gao, K., Yang, X., Jiang, Z. and Wang, L., 2022. Intestinal morphology and immune profiles are altered in piglets by early-weaning. International Immunopharmacology, 105, 108520. https://doi.org/10.1016/j.intimp.2022.108520

Coble, K.F., Burnett, D.D., DeRouchey, J.M., Tokach, M.D., Gonzalez, J.M., Wu, F., Dritz, S.S., Goodband, R.D., Woodworth, J.C. and Pluske, J.R., 2018. Effect of diet type and added copper on growth performance, carcass characteristics, energy digestibility, gut morphology, and mucosal mRNA expression of finishing pigs. Journal of Animal Science, 96(8), pp. 3288–3301. https://doi.org/10.1093/jas/sky196

Di Giancamillo, A., Rossi, R., Martino, P.A., Aidos, L., Maghin, F., Domeneghini, C. and Corino, C., 2018. Copper sulphate forms in piglet diets: Microbiota, intestinal morphology and enteric nervous system glial cells. Animal Science Journal, 89(4), pp. 616–624. https://doi.org/10.1111/asj.12948

Diao, H., Yan, J., Li, S., Kuang, S., Wei, X., Zhou, M., Zhang, J., Huang, C., He, P. and Tang, W., 2021. Effects of Dietary Zinc Sources on Growth Performance and Gut Health of Weaned Piglets. Frontiers in Microbiology, 12, 771617. https://doi.org/10.3389/fmicb.2021.771617

Dove, C.R., 1995. The effect of copper level on nutrient utilization of weanling pigs. Journal of Animal Science, 73(1), pp. 166–171. https://doi.org/10.2527/1995.731166x

Egger, M., Smith, G.D., Schneider, M. and Minder, C., 1997. Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109), p. 629. https://doi.org/10.1136/bmj.315.7109.629

Elliott, S., Frio, A. and Jarman, T., 2017. Heavy metal contamination of animal feedstuffs – a new survey. Journal of Applied Animal Nutrition, 5, e8. https://doi.org&10.1017/jan.2017.7

Espinosa, C.D., Fry, R.S., Kocher, M.E. and Stein, H.H., 2019. Effects of copper hydroxychloride and distillers dried grains with solubles on intestinal microbial concentration and apparent ileal and total tract digestibility of energy and nutrients by growing pigs. Journal of Animal Science, 97(12), pp. 4904–4911. https://doi.org/10.1093/jas/skz340

Espinosa, C.D., Fry, R.S., Usry, J.L. and Stein, H.H., 2017. Copper hydroxychloride improves growth performance and reduces diarrhea frequency of weanling pigs fed a corn–soybean meal diet but does not change apparent total tract digestibility of energy and acid hydrolyzed ether extract. Journal of Animal Science, 95(12), pp. 5447–5454. https://doi.org/10.2527/jas2017.1702

Espinosa, C.D. and Stein, H.H., 2021. Digestibility and metabolism of copper in diets for pigs and influence of dietary copper on growth performance, intestinal health, and overall immune status: a review. Journal of Animal Science and Biotechnology, 12(1), 13. https://doi.org/10.1186/s40104-020-00533-3

Feng, J., Ma, W.Q., Gu, Z.L., Wang, Y.Z. and Liu, J.X., 2007. Effects of Dietary Copper (II. Sulfate and Copper Proteinate on Performance and Blood Indexes of Copper Status in Growing Pigs. Biological Trace Element Research, 120(1-3), pp. 171–178. https://doi.org/10.1007/s12011-007-8001-y

Fry, R.S., Ashwell, M.S., Lloyd, K.E., O’Nan, A.T., Flowers, W.L., Stewart, K.R. and Spears, J.W., 2012. Amount and source of dietary copper affects small intestine morphology, duodenal lipid peroxidation, hepatic oxidative stress, and mRNA expression of hepatic copper regulatory proteins in weanling pigs. Journal of Animal Science, 90(9), pp. 3112–3119. https://doi.org/10.2527/jas.2011-4403

Galiotto Miranda, P.A., Remus, A., Dalto, D.B., Hilgemberg, R., Beber Jasluk, G., Rosário Silva, B.C. and Lehnen, C.R., 2024. A Systematic Review and Meta-Analysis of the Effects of Various Sources and Amounts of Copper on Nursery Piglets. Veterinary Sciences, 11(2), 68. https://doi.org/10.3390/vetsci11020068

Higgins, J.P.T. and Thompson, S.G., 2002. Quantifying heterogeneity in a meta-analysis. Statistics in Medicine, 21(11), pp. 1539–1558. https://doi.org/10.1002/sim.1186

Hill, G., ed.. 2023. Sustainable Swine Nutrition. 2nd edn. John Wiley & Sons Ltd.

Holman, D.B. and Chénier, M.R., 2015. Antimicrobial use in swine production and its effect on the swine gut microbiota and antimicrobial resistance. Canadian Journal of Microbiology, 61(11), pp. 785–798. https://doi.org/10.1139/cjm-2015-0239

Huting, A.M.S., Middelkoop, A., Guan, X. and Molist, F., 2021. Using Nutritional Strategies to Shape the Gastro-Intestinal Tracts of Suckling and Weaned Piglets. Animals, 11(2), 402. https://doi.org/10.3390/ani11020402

Ketata, M.A., Létourneau-Montminy, M.-P. and Guay, F., 2023. Estimation of digestible zinc and copper in pigs: a meta-analysis approach. Canadian Journal of Animal Science, 103(4), pp. 418-433. https://doi.org/10.1139/cjas-2023-0064

Lauridsen, C., Matte, J.J., Lessard, M., Celi, P. and Litta, G., 2021. Role of vitamins for gastro-intestinal functionality and health of pigs. Animal Feed Science and Technology, 273, 114823. https://doi.org/10.1016/j.anifeedsci.2021.114823

Lee, S., Hosseindoust, A., Goel, A., Choi, Y., Kwon, I.K., and Chae, B., 2016. Effects of dietary supplementation of bacteriophage with or without zinc oxide on the performance and gut development of weanling pigs. Italian Journal of Animal Science, 15, 412–418. https://doi.org/10.1080/1828051X.2016.1188676

Lewis, E.D., Meydani, S.N. and Wu, D., 2019. Regulatory role of vitamin E in the immune system and inflammation. IUBMB Life, 71(4), pp. 487–494. https://doi.org/10.1002/iub.1976

Li, J., Yan, L., Zheng, X., Liu, G., Zhang, N. and Wang, Z., 2008. Effect of high dietary copper on weight gain and neuropeptide Y level in the hypothalamus of pigs. Journal of Trace Elements in Medicine and Biology, 22(1), pp. 33–38. https://doi.org/10.1016/j.jtemb.2007.10.003

Liu, Y., Ma, Y.L., Zhao, J.M., Vazquez-Añón, M. and Stein, H.H., 2014. Digestibility and retention of zinc, copper, manganese, iron, calcium, and phosphorus in pigs fed diets containing inorganic or organic minerals. Journal of Animal Science, 92(8), pp. 3407–3415. https://doi.org/10.2527/jas.2013-7080

Manto, M., 2014. Abnormal Copper Homeostasis: Mechanisms and Roles in Neurodegeneration. Toxics, 2(2), pp. 327–345. https://doi.org/10.3390/toxics2020327

Moreira, R.H.R., Pérez Palencia, J.Y., Moita, V.H.C., Caputo, L.S.S., Saraiva, A., Andretta, I., Ferreira, R.A. and de Abreu, M.L.T., 2020. Variability of piglet birth weights: A systematic review and meta-analysis. Journal of Animal Physiology and Animal Nutrition, 104(2), pp. 657–666. doi.org. https://doi.org/10.1111/jpn.13264

National Research Council, 2012. Nutrient requirements of swine. 11th edn. Washington: National Academies Press.

Palencia, J.Y.P., Lemes, M.A.G., Garbossa, C.A.P., Abreu, M.L.T., Pereira, L.J. and Zangeronimo, M.G., 2018. Arginine for gestating sows and foetal development: A systematic review. Journal of Animal Physiology and Animal Nutrition, 102(1), pp. 204–213. https://doi.org/10.1111/jpn.12679

Pluske, J.R., Turpin, D.L. and Kim, J.-C., 2018. Gastrointestinal tract (gut. health in the young pig. Animal Nutrition, 4(2), pp. 187–196. https://doi.org/10.1016/j.aninu.2017.12.004

Sampath, V., Sureshkumar, S., Seok, W.J. and Kim, I.H., 2023. Role and functions of micro and macro-minerals in swine nutrition: a short review. Journal of Animal Science and Technology, 65(3), pp. 479–489. https://doi.org/10.5187/jast.2023.e9

Sandström, B., 2001. Micronutrient interactions: effects on absorption and bioavailability. British Journal of Nutrition, 85(S2), pp. S181-S185. https://doi.org/10.1049/BJN2000312

Smith II, J.W., Tokach, M.D., Goodband, R.D., Nelssen, J.L. and Richert, B.T., 1997. Effects of the interrelationship between zinc oxide and copper sulfate on growth performance of early-weaned pigs2. Journal of Animal Science, 75, pp.1861–1866. https://doi.org/10.2527/1997.7571861x

Tang, Q., Lan, T., Zhou, C., Gao, J., Wu, L., Wei, H., Li, W., Tang, Z., Tang, W., Diao, H., Xu, Y., Peng, X., Pang, J., Zhao, X., Sun, Z., 2024. Nutrition strategies to control post-weaning diarrhea of piglets: From the perspective of feeds. Animal Nutrition, 17, pp.297-311. https://doi.org/10.1016/j.aninu.2024.03.006

Tang, W., Qian, Y., Yu, B., Zhang, T., Gao, J., He, J., Huang, Z., Zheng, P., Mao, X., Luo, J., Yu, J., Chen, D., 2019. Effects of Bacillus subtilis DSM32315 supplementation and dietary crude protein level on performance, gut barrier function and microbiota profile in weaned piglets1. Journal Animal Science, 97, 2125–2138. https://doi.org/10.1093/jas/skz090

Veum, T.L., Carlson, M.S., Wu, C.W., Bollinger, D.W., Ellersieck, M.R., 2004. Copper proteinate in weanling pig diets for enhancing growth performance and reducing fecal copper excretion compared with copper sulfate1. Journal Animal Science, 82, pp.1062–1070. https://doi.org/10.1093/ansci/82.4.1062

Wang, J., Zhu, X., Guo, Y., Wang, Z., Zhao, B., Yin, Y., Liu, G., 2016. Influence of Dietary Copper on Serum Growth-Related Hormone Levels and Growth Performance of Weanling Pigs. Biological Trace Element Research, 172, pp.134–139. https://doi.org/10.1007/s12011-015-0574-2

Wang, M., Wang, Lixia, Tan, X., Wang, Lei, Xiong, X., Wang, Y., Wang, Q., Yang, H., Yin, Y., 2022. The developmental changes in intestinal epithelial cell proliferation, differentiation, and shedding in weaning piglets. Animal Nutrition, 9, pp.214–222. https://doi.org/10.1016/j.aninu.2021.11.006

Wang, M.-Q., Du, Y.-J., Wang, C., Tao, W.-J., He, Y.-D., Li, H., 2012. Effects of Copper-Loaded Chitosan Nanoparticles on Intestinal Microflora and Morphology in Weaned Piglets. Biological Trace Element Research, 149, pp.184–189. https://doi.org/10.1007/s12011-012-9410-0

Wang, Z., Li, J., Wang, Y., Wang, L., Yin, Yuebang, Yin, L., Yang, H., Yin, Yulong, 2020. Dietary vitamin A affects growth performance, intestinal development, and functions in weaned piglets by affecting intestinal stem cells. Journal Animal Science, 98, pp.skaa020. https://doi.org/10.1093/jas/skaa020

Wen, Y., Li, R., Piao, X., Lin, G., He, P., 2022. Different copper sources and levels affect growth performance, copper content, carcass characteristics, intestinal microorganism and metabolism of finishing pigs. Animal Nutrition, 8, 321–330. https://doi.org/10.1016/j.aninu.2021.10.007

Xia, J., Fan, H., Yang, J., Song, T., Pang, L., Deng, H., Ren, Z., Deng, J., 2022. Research progress on diarrhoea and its mechanism in weaned piglets fed a high-protein diet. Journal Animal Physiology Animal Nutrition (Berl), 106, pp.1277–1287. https://doi.org/10.1111/jpn.13654

Zhou, W., Kornegay, E.T., van Laar, H., Swinkels, J.W.G.M., Wong, E.A., Lindemann, M.D., 1994. The role of feed consumption and feed efficiency in copper-stimulated growth. Journal of Animal Science, 72, pp.2385–2394. https://doi.org/10.2527/1994.7292385x




URN: http://www.revista.ccba.uady.mx/urn:ISSN:1870-0462-tsaes.v29i2.56188

DOI: http://dx.doi.org/10.56369/tsaes.5618

Copyright (c) 2026 Victoria Tufiño-Loza, Renan Mena-Pérez, Diego Rodriguez-Saldaña, Jimmy Rolando Quisirumbay

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