Effect of dietary copper levels on the growth performance and nutrient utilization in fattening pigs

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1 B- 956 [1-5] Indian J. Anim. Res., Print ISSN: / Online ISSN: AGRICULTURAL RESEARCH COMMUNICATION CENTRE Effect of dietary copper levels on the growth performance and nutrient utilization in fattening pigs Seidu Adams 1, Meng Hongjiao 1, Dongsheng Che* 1, Jiang Hailong 1, Han Rui 1, Zhao Bao 1, Kofi Danquah 2 and Qin Guixin 1 College of Animal Science and Technology, Jilin Agricultural University, Changchun, China, Received: Accepted: DOI: /ijar.B-956 ABSTRACT The present study was conducted to investigate the effect of dietary copper supplementation on the growth performance, nutrient digestibility and copper metabolism in fattening pigs. A total of 24 pigs (Landrace X Large White X Duroc) with an average initial BW of 30±1.05 kg, the pigs were divided into four treatment groups, with three replicates per treatment and two pigs per replicate, in accordance with a completely randomized design based on the BW. The results indicated that dietary copper supplementation increased the growth performance, CP and EE digestibility. However, there was no significant increase in the DM and OM digestibility. In addition, copper deposition increased with the increase in dietary copper supplementation, while copper absorption, increased with the decrease in dietary copper levels. In conclusion, fattening pigs with BW can utilize mg/kg Cu and porkers at BW of kg can also utilize mg/kg Cu as CuSO4 for an increased copper utilization and a decreased in copper deposition. Key words: Copper, Digestibility, Metabolism, Performance, Pigs. INTRODUCTION Copper is an indispensable cofactor of enzymatic and non-enzymatic copper-dependent proteins that are required for mitochondrial respiration, neurotransmitter synthesis, peptide amidation, connective tissue formation, pigmentation, and iron metabolism, but due to its high toxicity when present in excessive amount, there is the need for subtle homeostatic balance of copper within cells (Yang et al. 2011). The growth stimulating effect of high copper concentrations is mainly observed in young pigs and its mode of action has been described by the antibacterial effects of high copper diets, making available more nutrients and energy in the gut for absorption (Blaabjerg and Poulsen 2017). A previous study has demonstrated the relationship between high dietary copper concentrations and improved growth performance in growing pigs (Feng et al. 2007). However, feeding high copper diets in growing pigs may result in the increased in copper accumulation in organs and excretion in manure, which poses both health and environmental risk (Kornegay and Verstegen 2001). Therefore, the present study examined the effects of dietary copper supplementation on the growth performance, nutrient digestibility, copper absorption and deposition in fattening pigs. MATERIALS AND METHODS A total of 24 (Landrace X Large White X Duroc) pigs with an average initial BW of 30±1.05 kg were selected for the current experiment. The experiment was conducted for 87 days, including 7 days of pre-feeding trial. The pigs were divided into four treatment groups, with three replicates per treatment and two pigs per replicate, arranged in accordance with a completely randomized design based on their BW. The pigs were housed individually in an environmentally-controlled room with an average temperature of 26 C. The houses were disinfected once a month, cleaned with a broom every day to keep a healthy and hygienic condition and prevent disease infection. The copper content in the treatments was adjusted based on the guidelines that stipulated that the diet of fattening pigs with live body weight between should contain 150 mg/kg copper and body weight above 60 kg should contain 25mg/kg copper. The control pigs were fed the basal diet and the experimental pigs were fed the basal diet with different copper concentrations. The diet was provided in a mash form and formulated in accordance to the NRC, (2012) nutrients requirement (Table 1). The pigs were fed in two different growth phases BW and kg BW. Pigs in the growing phase () were fed the basal diet with added copper levels of 10 mg/kg (control), 45 mg/kg (group 1), 135 mg/kg (group 2), and 225 mg/kg (group 3) copper and the fattening / porkers ( kg) pigs were fed the basal diet with added copper levels of 45 mg/kg, 135 mg/kg and 225 mg/kg. Chromium oxide (Cr 2 ) was used as a marker and added to all diets at 1% on day 33 to 40, and 80 to 87 of each feeding period in order to determine the digestibility values by the total collection method (Gonzales- Eguia et al., 2009). The basal diet contains corn-soybean *Corresponding author s chedongsheng@163.com 1 College of Animal Science and Technology, Jilin Agricultural University, Changchun, China, School of Allied Health Sciences, Department of Nutritional Sciences, University for Development Studies, Ghana 1350

2 2 INDIAN JOURNAL OF ANIMAL RESEARCH Table 1: Composition of experimental diets and nutrient indexes (%DM basis) Items 30 60kg 60kg -120kg Ingredients Corn Soybean meal Bran Bone meal Limestone Salt Lysine-HCL 0.2 Trace mineral premix Total Nutrient level Digestibility energy (MJ / kg) Crude protein (CP) Lysine (Lys) Methionine + Cysteine (Met+Cys) Copper sulphate (CuSO4)(mg/kg) Phosphorus (P) Calcium (Ca) Note: per kilogram of premix contains: iron 10000mg, zinc 1000mg, manganese 1000mg, selenium 30mg, iodine 50mg, VA IU, VD20000IU vitamin D2000IU, 2000mg niacin, folic acid, pantothenic acid 2000mg 30mg, VK50mg, riboflavin 250mg, VB1 200mg VB ug, choline chloride 100g, antioxidant 20000mg, biotin 5mg, VB6100mg. meal and dietary copper was supplemented as copper sulphate (CuSO 4 ). The pigs were provided with two equal meals daily about 5% of their live body weight, leftover feeds are collected, weigh and recorded. Water was supplied ad libitum throughout the entire experimental period. The feed consumption and body weight were determined weekly to calculate for the average daily feed intake per day (ADFI), average daily gain (ADG), and feed conversion ratio (FCR) for each phase ( and kg). The ADFI was estimated by totaling the quantity of feed wastage and the amount of feed left in the trough the next day, divided by the sum of piglets per pen. The feed intake divided by the weight gain to obtain the FCR. The pigs were weighed early in the morning on the last day of the feeding trial on an empty stomach to obtain the final weight. The initial weight subtracted from the final weight and divided by the test period of 80 days to give the ADG. The urine and fecal samples from the pigs were collected every day from day 33 to 40, and 80 to 87 for the determination of digestibility and copper deposition. The fecal samples were collected through total collection method and urine were taken on plastics then pooled within the pens into containers, 10 ml H 2 SO 4 (10 %v/v) was added to the urine and five drops of methylbenzene were added to prevent decomposition (Canh, et al., 1998; Mydland, et al., 2008), covered with lids. The feeds and feces were oven-dried at 55 C to obtain a constant weight and then ground to pass a 1-mm screen and store for further analysis. All samples were stored at -20 C for chemical analysis. The CP were estimated by the Kjeldahl method, and ether extract (EE) by the Soxhlet ether extraction apparatus, organic matter (OM) and dry matter (DM) as described by the AOAC, (2000). The copper concentrations in the feed, feces and urine were estimated in the laboratory using flame atomic absorption spectrophotometry as previously described (Huang et al. 2010a). The digestibility of copper and copper deposition were calculated as follows: Copper digestibility = [100 - [(amount of Cr 2 in feed) (amount of Cr 2 in the feces)] X [(amount of copper in the feces) (amount of copper in the feed)] X 100]. Copper deposition rate = [(copper content in the feed copper content in the feces copper content in the urine) (copper content in the feed) X 100]. The data were analyzed by oneway analysis of variance (ANOVA) using SPSS version 13.0 (SPSS Inc., Chicago, IL, USA). A probability value of P 0.05 was considered to be statistically significant and the multiple comparison test was performed by LSD method, the test results were estimated as Mean ± SE. RESULTS AND DISCUSSION The growth performance is presented in Table 2. In the BW, the results showed that the production performance of test group 3 was significantly higher (p<0.05) and recorded a significantly lower FCR in comparison with the control. In the kg, the ADFI of groups 2 and 3 was significantly higher (p<0.05) and the control group recorded the lowest (p>0.05) ADG level. However, the FCR (p<0.05) in the experimental groups was higher than the control. In the entire growth phase ( kg), the control group recorded the lowest ADFI, ADG, and FCR. There was an increased in ADFI, ADG, and FCR in group 1, group 2, and group 3 but not significantly different from the control (p>0.05). However, the ADG level in group 3 was significantly different from the control (p<0.05). A previous study has shown that higher copper diets increased the growth performance of pigs (Feng et al. 2007), and the current study testified that higher dietary supplementation of copper as copper sulphate increased the growth performance of fattening pigs but not significantly different from the control. Similar to this finding was the study of Veum et al. (2004), who observed that 200 ppm of copper-proteinate and 250 ppm of copper sulphate provided in the diet of weaning piglets increased the growth performance but not significantly higher than the control after feeding for 28 days. Also, Huang et al. (2010a), who determined that 134 ppm of four different copper diets fed to growing pigs for 35 days increased the growth performance but not significantly higher than the control. Contrarily to our results, Stansbury et al. (1990) determined that there was no increased in the ADFI or ADG in weanling pigs fed on 125 or 250 ppm copper as copper sulphate. Also, Dove and Ewan (1990), reported that there was no significant increase in ADFI, ADG, and FCR in growing pigs after dietary copper supplementation.

3 Vol. Issue, () Table 2: Effect of dietary copper levels on growth performance of fattening pigs Parameters Control Group 1 Group 2 Group 3 ADFI /g ±4.89 b ±5.61 b ±6.21 ab ±3.25 a ADG/g ±1.65 b ±3.16 b ±2.81 ab ± 2.45 a FCR 3.51±0.05 ab 3.25±0.04 a 3.21±0.02 a 3.05±0.01 a kg ADFI /g ±2.52 a ±2.10 a ±2.31 ab ±3.21 ab ADG/g ±2.24 a ±3.12 a ±1.25 a ±1.85 a FCR 4.45±3.64 c 4.61±2.61 b 4.83±1.71 a 5.26±2.53 a kg ADFI /g ±2.67 ab ±5.0 a ±2.62 a ±3.80 a ADG/g ±5.31 b ±4.84 b ±5.02 ab ±7.52 a FCR 2.73±0.02 a 2.84±0.15 ab 2.76±0.21 a 2.91±0.07 ab Note: different letters within the same row represent significant difference. Control= 10 mg/kg Cu, Group 1= 45 mg/kg Cu, Group 2= 135 mg/kg Cu, and Group 3= 225 mg/kg Cu Table 3: Effect of dietary copper levels on nutrient digestibility of finishing pigs Parameters Control Group 1 Group 2 Group 3 CP 89.39±2.14 a 88.04±1.42 a 87.93±1.56 a 86.21±1.91 a EE 14.01±4.32 a 21.60±7.25 b 30.52±8.21 bc 32.65±1.20 c DM 89.48±2.24 a 88.65±0.51 a 89.18±2.01 a 91.20±0.25 a OM 92.31±0.58 a 91.31±0.89 a 91.72±0.97 a 92.21±0.25 a kg CP 85.21±1.65 b 86.64±1.65 b 87.62±1.35 ab 90.12±2.15 a EE 13.24±3.21 c 19.31±5.21 b 29.31±3.21 a 30.65±3.21 a DM 90.25±2.20 a 89.21±0.21 a 89.25±1.15 a 90.20±2.20 a OM 90.21±2.21 a 90.32±0.65 a 92.25±0.85 a 90.25±0.27 a Note: different letters within the same row represent significant difference. Control= 10 mg/kg Cu, Group 1= 45 mg/kg Cu, Group 2= 135 mg/kg Cu, and Group 3= 225 mg/kg Cu It is an established fact that high dietary copper levels can promote the digestibility of crude fat, crude protein, and the absorption capacity of the digestive tract of swine (Gonzales-Eguia et al., 2009). As shown in Table 3, the digestibility of CP decreased with the increase in dietary copper levels in the BW. The digestibility of CP was higher (p>0.05) in the control group while EE digestibility was significantly low (p<0.05) in the control group in comparison with the treatment groups. There was no significant difference (p>0.05) in the DM and OM digestibility among the treatment groups. In the kg BW, the digestibility of CP and EE increased with the corresponding increase in copper levels in the basal diet. As a result of the increased in maturity of the gastrointestinal tract, increase in dietary copper level increased the antibiotic effects of copper (Hawbaker et al. 1961; Huang et al. 2010a) therefore increasing microbial growth, composition and activities in the intestines (Cromwell, 2001). Hence increasing the digestibility of DM, CP and EE. The DM and OM digestibility in the 10 mg/kg and 135 mg/kg copper diet increased (P> 0.05) respectively. Similar to the current result, Huang et al. (2010b) indicated that DM digestibility was not affected by 134 ppm copper supplementation at the end of the 21 days of feeding growing pigs, but was significantly improved at the end of the 35 days of feeding. Also, there was no significant difference in DM digestibility as indicated by (Huang et al. 2010a). Contrary to this current results was the previous study by Dove (1995), who determined that 250 ppm copper supplementation significantly increased DM and OM digestibility in weanling pigs. As shown in Table 4, copper intake, fecal copper excretion, copper deposition, and copper digestibility in kg BW pigs increased first and then decreased with the increase in dietary copper levels. That is when dietary copper dosage was mg/kg (P <0.01), there was a significant difference between the control group and the experimental group 3 in copper intake, fecal copper excretion, and copper deposition in vivo. The rate of copper intake in the 225 mg/ kg treatment was 6.75 times higher, 3.5 times higher in copper deposition, 5.4 times higher in fecal copper excretion and 10 times higher in urinary copper excretion than the control. Hence, indicating that high copper diets significantly increased total copper deposition and excretion in pigs. The digestibility of copper in group 1 and group 2 was significantly higher than that in the control group and group

4 4 INDIAN JOURNAL OF ANIMAL RESEARCH Table 4: The rate of copper deposition and digestibility in fattening pigs Treatments Feed Copper Copper Fecal Copper Urinary Copper Copper Copper Rate of Content(g/d) Intake (g/d) Content (g/d) Content (g/d) Deposition digestibility Copper (g/d) (%) deposition (%) Control ± ± ± ± ± ± ±0.20 Group ± ± ± ± ± ± ±0.33 Group ± ± ± ± ± ± ±0.21 Group ± ± ± ± ± ± ± kg Control ± ± ± ± ± ± ± 0.21 Group ± ± ± ± ± ± ±0.20 Group ± ± ± ± ± ± ± 0.17 Group ± ± ± ± ± ± ± 0.31 Control= 10 mg/kg Cu, Group 1= 45 mg/kg Cu, Group 2= 135 mg/kg Cu, and Group 3= 225 mg/kg Cu 3 (P<0.05) at BW. It was observed that dietary copper supplementation at 45 mg/kg and 135 mg/kg increased copper digestibility in fattening pigs. There was a significant difference (P<0.01) between the control and 225 mg/kg group at kg BW (Table 4). The supplementation of copper at 225 mg/kg increased the rate of copper intake in pigs was 7.22 times higher, copper deposition was 10 times higher, fecal copper excretion was 22 times higher and urinary copper excretion was 13 times higher than the control. However, the digestibility of copper in the control group and the 45 mg/ kg copper was significantly higher (p<0.05) than the 135 mg/kg and the 225 mg/kg treatments. Hence indicating that the addition of mg/kg dietary copper can improve the copper digestibility in finishing pig s. Comparatively, the fecal copper excretion in the kg BW pigs was higher than the BW pigs, indicating that the rate of copper metabolism was low at higher body mass. Similarly, Wapnir (1998) showed that about 20% of the copper contained in feed materials was absorbed by the digestive tract, while 60% of the absorbed copper was released into the digestive tract with bile. Also, Apgar and Kornegay (1996) observed higher levels of copper in the feces and urine of pigs fed higher copper levels from both copper-lysine and copper sulphate. The same authors observed that pigs fed higher copper diet absorbed more copper than pigs fed lower copper diet. The results of this study indicated that copper deposition increased with the increase in dietary copper levels. Therefore, the findings of this studies showed that dietary copper supplementation within the ranges of 45 mg/ kg to 135 mg/kg increased copper digestibility and decreased copper deposition rate in BW of fattening pigs, while 10 mg/kg to 45 mg/kg was a convenient range for the increased in copper digestibility and decreased in copper deposition in kg BW of fattening pigs CONCLUSION The increase in copper content of the diet increased the growth performance, crude protein and ether extract digestibility in fattening pigs. However, higher copper concentrations increased fecal and urinary copper excretion. Hence decreasing the digestibility of copper and increasing its deposition in the body. The findings of this current study indicate that at a body weight between, fattening pigs should be given dietary copper levels between 45 mg/ kg to 135 mg/kg. While, at the porker phase of kg, fattening pigs should be fed with 10 mg/kg copper to 45 mg/ kg copper. As these ranges increased production and copper digestibility, while decrease copper deposition DECLARATION OF INTEREST The authors declare that there is no conflict of interest ACKNOWLEDGEMENT Thanks to the National Key Research and Development Program of China (2017YFD ) and the Scientific Project of Jilin Province ( NY & JC) for providing financial support for publishing this article. REFERENCE AOAC. ( 2000). Association of Official Analytical Chemists. Official Methods of Analysis. Ed. Arlington VA. Apgar, G. A., Kornegay, E. T. (1996). Mineral balance of finishing pigs fed copper sulfate or a copper-lysine complex at growthstimulating levels1. Journal of Animal Science 74: Blaabjerg, K. and Poulsen, H. D. (2017). The use of zinc and copper in pig production. Nationalt Center for Jordbrug og Fødevarer. Canh, T., Aarnink, A., Schutte, J., Sutton, A., Langhout, D., Verstegen, M., (1998). Dietary protein affects nitrogen excretion and ammonia emission from slurry of growing-finishing pigs. Livestock Production Science 56: Cromwell, G. L. (2001). Antimicrobial and promicrobial agents. In Swine Nutrition. 2nd ed. (Ed. A. J. Lewis and L. L. Southern). CRC Press LLC, Boca Raton, FL Dove, C. R. (1995). The effect of copper level on nutrient utilization of weanling pigs. Journal of Animal Science 73:

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