Zinc supplementation improves growth performance in small ruminants: a systematic review and meta-regression analysis
J. C. Angeles-Hernandez A , M. Miranda B , A. L. Muñoz-Benitez A , R. Vieyra-Alberto A , N. Morales-Aguilar A , E. A. Paz C and M. Gonzalez-Ronquillo D EA Instituto de Ciencias Agropecuarias, Universidad Autónoma del Estado de Hidalgo, Av. Universidad km 1, Tulancingo de Bravo, Hidalgo 43600, México.
B Departamento de Anatomía, Producción Animal y Ciencias Clínicas Veterinarias, Facultad de Veterinaria, Universidad de Santiago de Compostela, 27002, Lugo, Spain.
C UWA Institute of Agriculture, The University of Western Australia, Crawley, WA 6009, Australia.
D Departamento de Producción Animal, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma del Estado de México. Instituto Literario n° 100, Col. Centro, Toluca 50000, México.
E Corresponding author. Email: mrg@uaemex.mx
Animal Production Science 61(7) 621-629 https://doi.org/10.1071/AN20628
Submitted: 12 November 2020 Accepted: 3 March 2021 Published: 12 April 2021
Abstract
Appropriate supplementation of trace minerals is fundamental to enhance the metabolic status of growing animals and promote an adequate expression of genetic potential. Zinc (Zn) is an essential mineral fundamental in many biological processes that are related to growth, energy balance and immunity. The aim of the present study was to analyse the effect of Zn supplementation on growth parameters in small ruminants by using a meta-analytic approach. Sources of heterogeneity were explored using a meta-regression analysis. The final database was integrated from a total of 53 trials. Only indexed articles that provided an effect size measure, variability measure, sample size and randomisation of the procedure were considered. The dependent variables considered for the study were average daily gain (ADG), dry-matter intake (DMI), feed conversion ratio (FCR), final bodyweight, and glucose blood concentration. The exploratory variables included species (sheep and goat), breed, production level, Zn source and dosage. The ‘meta’ package in R statistical software was used to conduct the meta-analyses. For response variables that showed substantial heterogeneity (I2 > 50%), mixed-effect models (meta-regression analysis) were constructed to explore the sources of heterogeneity using the ‘Metafor’ package. DMI was higher in animals supplemented with Zn (>21.08 g/day, P = 0.0001). Breed, species, production level, and dosage reduced heterogeneity of DMI response from I2 = 84.8 to I2 = 48.1%. Zn-supplemented animals showed higher ADG (17.39 g/day, P = 0.001), which was affected by species, breed dosage and Zn-source. Zn supplementation improved feed efficiency, with lower values of FCR (–1.56 g/g, P < 0.0001). There was a positive relationship between the dosage and effect size in all outcome variables (P < 0.05). Zn-proteinate showed the best response in both species to ADG, FCR and final body weight. Our findings of the systematic review concluded that dietary Zn supplementation improves growth performance in small ruminants and their level of response is influenced mainly by species, production level, and Zn-source and dosage.
Keywords: zinc, goats, sheep.
References
Abdelrahman MM, AL-Rayyan NAM, Awawdeh FT, Alazzeh AY (2003) The Effect of Dietary Levels of Zinc-Methionine on the Performance of Growing Awassi Lambs. Pakistan Journal of Biological Sciences 6, 979–983.| The Effect of Dietary Levels of Zinc-Methionine on the Performance of Growing Awassi Lambs.Crossref | GoogleScholarGoogle Scholar |
Aditia M, Sunarso , Sevilla CC, Angeles AA (2014) Growth performance and mineral status on goats (Capra hircuslinn) supplemented with zinc proteinate and selenium yeast. International Journal of Science and Engineering 7, 124–129.
| Growth performance and mineral status on goats (Capra hircuslinn) supplemented with zinc proteinate and selenium yeast.Crossref | GoogleScholarGoogle Scholar |
Aliarabi H, Fadayifar A, Tabatabaei MM, Zamani P, Bahari A, Farahavar A, Dezfoulian AH (2015) Effect of Zinc Source on Hematological, Metabolic Parameters and Mineral Balance in Lambs. Biological Trace Element Research 168, 82–90.
| Effect of Zinc Source on Hematological, Metabolic Parameters and Mineral Balance in Lambs.Crossref | GoogleScholarGoogle Scholar | 25910899PubMed |
Alimohamady R, Aliarabi H, Bruckmaier RM, Christensen RG (2019) Effect of Different Sources of Supplemental Zinc on Performance, Nutrient Digestibility, and Antioxidant Enzyme Activities in Lambs. Biological Trace Element Research 189, 75–84.
| Effect of Different Sources of Supplemental Zinc on Performance, Nutrient Digestibility, and Antioxidant Enzyme Activities in Lambs.Crossref | GoogleScholarGoogle Scholar | 30032401PubMed |
Appuhamy JADRN, Strathe AB, Jayasundara S, Dijkstra J, France J, Kebreab E (2013) Anti-methanogenic effects of monensin in dairy and beef cattle: a meta-analysis. Journal of Dairy Science 96, 5161–5173.
| Anti-methanogenic effects of monensin in dairy and beef cattle: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Cao J, Henry PR, Guo R, Holwerda RA, Toth JP, Littell RC, Ammerman CB (2000) Chemical characteristics and relative bioavailability of supplemental organic zinc sources for poultry and ruminants. Journal of Animal Science 78, 2039–2054.
| Chemical characteristics and relative bioavailability of supplemental organic zinc sources for poultry and ruminants.Crossref | GoogleScholarGoogle Scholar | 10947086PubMed |
Chavan SJ, Varadan D, Ravishankar C, Vazhoor B, Sebastian R, Chulliparambil S, Prakash P (2021) The Effect of Inorganic and Organic Zinc Supplementation on Growth Performance, Mineral Profile and Gene Expression Pattern of GLUT1 in Malabari Kids. Biological Trace Element Research 199, 568–577.
| The Effect of Inorganic and Organic Zinc Supplementation on Growth Performance, Mineral Profile and Gene Expression Pattern of GLUT1 in Malabari Kids.Crossref | GoogleScholarGoogle Scholar | 32363521PubMed |
Cousins RB, Liuzzi JP, Lichten LA (2006) Mammalian zinc transport, trafficking and signals. The Journal of Biological Chemistry 281, 24085–24089.
| Mammalian zinc transport, trafficking and signals.Crossref | GoogleScholarGoogle Scholar |
Dalenius T, Hodges JL (1959) Minimum variance stratification. Journal of the American Statistical Association 54, 88–101.
DerSimonian R, Laird N (2015) Meta-Analysis in Clinical Trials revisited. Contemporary Clinical Trials 45, 139–145.
| Meta-Analysis in Clinical Trials revisited.Crossref | GoogleScholarGoogle Scholar | 26343745PubMed |
Elamin KM, Dafalla NA, Abdel AKA, Atameem EA (2013) Effects of Zinc Supplementation on Growth Performance and some Blood Parameters of Goat Kids in Sudan. International Journal of Pure and Applied Biological Research and Science 1, 1–8.
Fadayifar A, Aliarabi H, Tabatabaei MM, Zamani P, Bahari A, Malecki M, Dezfoulian AH (2012) Improvement in lamb performance on barley based diet supplemented with zinc. Livestock Science 144, 285–289.
| Improvement in lamb performance on barley based diet supplemented with zinc.Crossref | GoogleScholarGoogle Scholar |
Farghaly MM, Mousa SM, Abd El-Hafez GA, Abd El-Rahman MA (2017) The effect of zinc supplementation of performance of growing lambs. Egyptian Journal of Nutrition and Feeds 20, 59–68.
| The effect of zinc supplementation of performance of growing lambs.Crossref | GoogleScholarGoogle Scholar |
Garg AK, Mudgal V, Dass RS (2008) Effect of organic zinc supplementation on growth nutrient utilization and mineral profile in lambs. Animal Feed Science and Technology 144, 82–96.
| Effect of organic zinc supplementation on growth nutrient utilization and mineral profile in lambs.Crossref | GoogleScholarGoogle Scholar |
Goff JP (2018) Invited review: mineral absorption mechanisms, mineral interactions that affect acid-base and antioxidant status, and diet considerations to improve mineral status. Journal of Dairy Science 101, 2763–2813.
| Invited review: mineral absorption mechanisms, mineral interactions that affect acid-base and antioxidant status, and diet considerations to improve mineral status.Crossref | GoogleScholarGoogle Scholar | 29397180PubMed |
Gotoh T (2015) Potential of the application of epigenetics in animal production. Animal Production Science 55, 145–158.
| Potential of the application of epigenetics in animal production.Crossref | GoogleScholarGoogle Scholar |
Grace ND (1984) The determination of mineral requirements of sheep and cattle. Proceedings of the New Zealand Society of Animal Production 44, 139–141.
Grace ND (2002) Role and importance of trace elements in New Zealand livestock, fact and fiction. Proceedings of the New Zealand Society of Animal Production 62, 311–314.
Grace ND, Watkinson JH (1988) Se, Cu, Zn and Fe metabolism of the young lamb. Proceedings of the New Zealand Society of Animal Production 48, 257–260.
Hedges LV (1981) Distribution Theory for Glass’s Estimator of Effect size and Related Estimators. Journal of Educational Statistics 6, 107–128.
| Distribution Theory for Glass’s Estimator of Effect size and Related Estimators.Crossref | GoogleScholarGoogle Scholar |
Higgins JPT (2008) Commentary: heterogeneity in meta-analysis should be expected and appropriately. International Journal of Epidemiology 37, 1158–1160.
| Commentary: heterogeneity in meta-analysis should be expected and appropriately.Crossref | GoogleScholarGoogle Scholar |
Higgins JPT, Green S (2011) Cochrane Handbook for Systematic Reviews of Interventions. Version 5.1.0. [updated March 2011]. London: Cochrane Collaboration. Available at www.handbook.cochrane.org.quantified [Verified 8 December 2019]
Jafarpour N, Khorvash M, Rahmani HR, Pezeshki A, Ghaffari H (2015) Dose–responses of zinc–methionine supplements on growth, blood metabolites and gastrointestinal development in sheep. Journal of Animal Physiology and Animal Nutrition 99, 668–75.
| Dose–responses of zinc–methionine supplements on growth, blood metabolites and gastrointestinal development in sheep.Crossref | GoogleScholarGoogle Scholar | 25580958PubMed |
Jia W, Jia Z, Zhang W, Wang R, Zhang S, Zhu X (2008) Effects of dietary zinc on performance, nutrient digestibility and plasma zinc status in Cashmere goats. Small Ruminant Research 80, 68–72.
| Effects of dietary zinc on performance, nutrient digestibility and plasma zinc status in Cashmere goats.Crossref | GoogleScholarGoogle Scholar |
Jia W, Zhu X, Zhang W, Cheng J, Guo C, Jia Z (2009) Effects of Source of Supplemental Zinc on Performance, Nutrient Digestibility and Plasma Mineral Profile in Cashmere Goats. Asian-Australasian Journal of Animal Sciences 22, 1648–1653.
| Effects of Source of Supplemental Zinc on Performance, Nutrient Digestibility and Plasma Mineral Profile in Cashmere Goats.Crossref | GoogleScholarGoogle Scholar |
Johnson T (2020) trtools: Miscellaneous Tools for Teaching Statistics. R package version 0.2.6. Available at http://github.com/trobinj/trtools
Kumar H, Tiwari SP, Sahu T, Naik SK, Doneria R (2015) Influence of zinc and chromium supplementation on growth and nutrient utilization in goats. Indian Journal of Small Ruminants 21, 40–45.
| Influence of zinc and chromium supplementation on growth and nutrient utilization in goats.Crossref | GoogleScholarGoogle Scholar |
Lean IJ, Thompson JM, Dunshea FR (2014) A Meta-Analysis of Zilpaterol and Ractopamine Effects on Feedlot Performance, Carcass Traits and Shear Strength of Meat in Cattle. PLoS One 9, e115904
| A Meta-Analysis of Zilpaterol and Ractopamine Effects on Feedlot Performance, Carcass Traits and Shear Strength of Meat in Cattle.Crossref | GoogleScholarGoogle Scholar | 25548908PubMed |
Lichti EL, Almond CH, Henzel JH, De Weese MS (1970) Differences in maternal and fetal plasma zinc levels in sheep and goats. American Journal of Obstetrics and Gynecology 106, 1242–1244.
| Differences in maternal and fetal plasma zinc levels in sheep and goats.Crossref | GoogleScholarGoogle Scholar | 5437817PubMed |
Mallaki M, Norouzian MA, Khadem AA (2015) Effect of organic zinc supplementation on growth, nutrient utilization, and plasma zinc status in lambs. Turkish Journal of Veterinary and Animal Sciences 39, 75–80.
| Effect of organic zinc supplementation on growth, nutrient utilization, and plasma zinc status in lambs.Crossref | GoogleScholarGoogle Scholar |
Morand-Fehr P, Fedele V, Decandia M, Le Frileux Y (2007) Influence of farming and feeding systems on composition and quality of goat and sheep milk. Small Ruminant Research 68, 20–34.
| Influence of farming and feeding systems on composition and quality of goat and sheep milk.Crossref | GoogleScholarGoogle Scholar |
Nafikov RA, Beitz CD (2007) Carbohydrate and Lipid Metabolism in Farm Animals. The Journal of Nutrition 137, 702–705.
| Carbohydrate and Lipid Metabolism in Farm Animals.Crossref | GoogleScholarGoogle Scholar | 17311965PubMed |
Pechova A, Misurova L, Pavlata L, Dvorak R (2009) The influence of supplementation of different forms of zinc in goats on the zinc concentration in blood plasma and milk. Biological Trace Element Research 132, 112–121.
| The influence of supplementation of different forms of zinc in goats on the zinc concentration in blood plasma and milk.Crossref | GoogleScholarGoogle Scholar | 19415185PubMed |
Puchala R, Sahlua T, Davis JJ (1999) Effects of zinc-methionine on performance of Angora goats. Small Ruminant Research 33, 1–8.
| Effects of zinc-methionine on performance of Angora goats.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2013. Available at http://www. r-project.org [Verified 12 December 2019]
Rodríguez-Maya MA, Domínguez-Vara IA, Trujillo-Gutiérrez D, Morales-Almaráz E, Sánchez-Torres JE, Bórquez-Gastelum JL, Acosta-Dibarrat J, Grageola-Nuñez F, Rodríguez-Carpena JG (2019) Growth performance parameters, carcass traits, and meat quality of lambs supplemented with zinc methionine and (or) zinc oxide in feedlot system. Canadian Journal of Animal Science 99, 585–595.
| Growth performance parameters, carcass traits, and meat quality of lambs supplemented with zinc methionine and (or) zinc oxide in feedlot system.Crossref | GoogleScholarGoogle Scholar |
Salama AA, Caja G, Albanell E, Such X, Casals R, Plaixats J (2003) Effects of dietary supplements of zinc-methionine on milk production, udder health and zinc metabolism in dairy goats. The Journal of Dairy Research 70, 9–17.
| Effects of dietary supplements of zinc-methionine on milk production, udder health and zinc metabolism in dairy goats.Crossref | GoogleScholarGoogle Scholar | 12617388PubMed |
Salamanca A (2010) Mineral supplementation for cattle production. Available at https://www.cabdirect.org/cabdirect/abstract/20113095664 [Verified 11 December 2019]
Schwarzer G (2016) Meta: General Package for Meta-Analysis. Available at https://cran.r-project.org/web/packages/meta/index.html [Verified 5 December 2019]
Sethy K, Behera K, Mishra SK, Gupta SK, Sahoo N, Parhi SS, Mahapatra MR, Khadanga S (2017) Effect of organic zinc supplementation on growth, metabolic profile and antioxidant status of Ganjam sheep. Indian Journal of Animal Research 99, 668–675.
| Effect of organic zinc supplementation on growth, metabolic profile and antioxidant status of Ganjam sheep.Crossref | GoogleScholarGoogle Scholar |
Solaiman SG, Min BR (2019) The effect of high levels of dietary zinc on growth performance, carcass characteristics, blood parameters, immune response and tissue minerals in growing Boer-cross goat kids. Small Ruminant Research 177, 167–174.
| The effect of high levels of dietary zinc on growth performance, carcass characteristics, blood parameters, immune response and tissue minerals in growing Boer-cross goat kids.Crossref | GoogleScholarGoogle Scholar |
Spears JW (1989) Zinc methionine for ruminants: relative bioavailability of zinc in lambs and effects of growth and performance of growing heifers. Journal of Animal Science 67, 835–846.
| Zinc methionine for ruminants: relative bioavailability of zinc in lambs and effects of growth and performance of growing heifers.Crossref | GoogleScholarGoogle Scholar | 2722712PubMed |
Suttle NF (2010) ‘Mineral Nutrition of Livestock.’ 4th edn. CAB International, Oxfordshire, UK.
Tang XH, Shay NF (2001) Zinc has an insulin-like effect on glucose transport mediated by phosphoinositol-3-kinase and Akt in 3T3-L1 fibroblasts and adipocytes. The Journal of Nutrition 131, 1414–1420.
Van Niekerk FE, Van Niekerk CH, Heine EWP, Coetzee J (1990) Concentrations of plasma copper and zinc and blood selenium in ewes and lambs of Merino, Dohne Merino and SA Mutton Merino sheep. South African Journal of Animal Science 20, 21–26.
Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package Journal of Statistical Software 36, 1–48.
| Conducting meta-analyses in R with the metafor packageCrossref | GoogleScholarGoogle Scholar |
Wang R, Zhu X, Guo F, Zhang W, Jia Z (2006) Influence of different dietary levels of zinc on performance, vitamin B12, and blood parameters in lambs. International Journal for Vitamin and Nutrition Research 76, 353–358.
| Influence of different dietary levels of zinc on performance, vitamin B12, and blood parameters in lambs.Crossref | GoogleScholarGoogle Scholar | 17607954PubMed |
Wedekind KJ, Hortin AE, Baker DH (1992) Methodology for assessing zinc bioavailability: Efficacy estimates for zinc methionine, zinc sulfate, and zinc oxide Journal of Animal Science 70, 178–187.
| Methodology for assessing zinc bioavailability: Efficacy estimates for zinc methionine, zinc sulfate, and zinc oxideCrossref | GoogleScholarGoogle Scholar | 1582905PubMed |
White CL, Chandler BS, Peter DW (1991) Zinc supplementation of lactating ewes and weaned lambs grazing improved mediterranean pastures. Australian Journal of Experimental Agriculture 31, 183–189.
| Zinc supplementation of lactating ewes and weaned lambs grazing improved mediterranean pastures.Crossref | GoogleScholarGoogle Scholar |
White CL (1992) Zinc deficiency in man and animals: endemic or imaginary. Proceedings of the Nutrition Society of Australia 17, 115–123.
Windisch W (2002) Interaction of chemical species with biological regulation of the metabolism of essential trace elements. Analytical and Bioanalytical Chemistry 372, 421–425.
| Interaction of chemical species with biological regulation of the metabolism of essential trace elements.Crossref | GoogleScholarGoogle Scholar | 11939527PubMed |
Wolf P, Groen EA, Berg W, Prochnow A, Bokkers EAM, Heijungs R (2017) Assessing greenhouse gas emissions of milk production: which parameters are essential? The International Journal of Life Cycle Assessment 22, 441–455.
| Assessing greenhouse gas emissions of milk production: which parameters are essential?Crossref | GoogleScholarGoogle Scholar |
Wright CL, Spears JW, Webb KE (2008) Uptake of zinc from zinc sulfate and zinc proteinate by ovine ruminal and omasal epithelia. Journal of Animal Science 86, 1357–1363.
| Uptake of zinc from zinc sulfate and zinc proteinate by ovine ruminal and omasal epithelia.Crossref | GoogleScholarGoogle Scholar | 18310488PubMed |