INTRODUCTION. Z. Kamran,* M. Sarwar,* 1 M. Nisa,* M. A. Nadeem, S. Mahmood, M. E. Babar, and S. Ahmed

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1 Effect of Low-Protein Diets Having Constant Energy-to-Protein Ratio on Performance and Carcass Characteristics of Broiler Chickens from One to Thirty-Five Days of Age Z. Kamran,* M. Sarwar,* 1 M. Nisa,* M. A. Nadeem, S. Mahmood, M. E. Babar, and S. Ahmed *Institute of Animal Nutrition and Feed Technology, University of Agriculture, Faisalabad, Pakistan 38040; Animal Nutrition, Animal Science Institute, National Agriculture Research Centre, Park Road, Islamabad, Pakistan 45500; Department of Poultry Science, University of Agriculture, Faisalabad, Pakistan; Department of Livestock Production, University of Veterinary and Animal Sciences, Lahore, Pakistan ABSTRACT A trial was conducted to determine the each diet was offered to 4 replicates at random. Weight effect of low-protein diets with constant ME:CP ratio on performance and carcass characteristics of broilers from 1 to 35 d of age. Four experimental diets were formulated to have 4 levels of CP and ME, respectively, in each phase: 23, 22, 21, and 20% CP with 3,036, 2,904, 2,772, and 2,640 kcal/kg in the starter phase (1 to 10 d); 22, 21, 20, and 19% CP with 3,146, 3,003, 2,860, and 2,717 kcal/kg in the grower phase (11 to 26 d); and 20, 19, 18, and 17% CP with 3,100, 2,945, 2,790, and 2,635 kcal/kg in the finisher phase (27 to 35 d). Digestible Lys was maintained at 1.10, 1.02, and 0.90% of the diet in the starter, grower, and finisher periods, respectively. A total of 1,760 one-dayold Hubbard broiler chickens were randomly divided into 16 experimental pens, 110 chickens in each pen, and gain was linearly decreased (P < 0.001), whereas feed intake and feed conversion ratio were increased (P < 0.001) linearly as dietary protein and energy decreased during grower, finisher, and overall experimental periods. Protein efficiency ratio and energy efficiency ratio were decreased (P < 0.05) with low-cp and low-me diets during the grower, finisher, and overall experimental period. However, carcass yield, breast meat yield, thigh yield, abdominal fat, and relative liver and heart weights were not affected by the treatments. Feeding broiler chickens low-cp diets with constant ME:CP ratio has adversely affected the growth performance, but carcass parameters were unaffected without any increase in abdominal fat content. Key words: low-protein diet, energy:protein ratio, broiler performance, carcass characteristic, abdominal fat 2008 Poultry Science 87: doi: /ps INTRODUCTION Lowering the CP content of broiler diets may reduce feed cost and allow for use of alternate feedstuffs. Some researchers have found that reducing dietary CP does not affect growth performance (Parr and Summers, 1991; Moran and Stilborn, 1996). However, rate and efficiency of growth is lower, and carcass composition becomes inferior in broilers fed diets in which CP has been lowered by more than 3%, even when all known nutrient requirements are met (Fancher and Jensen, 1989; Aletor et al., 2000; Bregendahl et al., 2002; Sterling et al., 2005; Waldroup et al., 2005). It is known that the CP and amino acid (AA) status of a diet influences the carcass composition of broilers, and decrease in dietary CP causes a decrease in carcass protein and an increase in carcass fat content (Si 2008 Poultry Science Association Inc. Received May 3, Accepted October 28, Corresponding author: zkami79@gmail.com et al., 2001). But it is questionable whether dietary energy intake plays a role in regulating lipogenesis in birds fed at a suboptimal regimen of protein nutrition. It is of interest to determine whether the high rate of lipogenesis and poor growth performance resulting from low-cp diets can be overcome by maintaining a constant ME:CP ratio. It is now well documented that dietary composition and the ratios between macronutrients have a major effect on performance and body composition of chickens (Buyse et al., 1992; Nieto et al., 1997; Collin et al., 2003). In general, diets with a high energy:protein ratio promote energy retention as fat; however, little is known about the use of low-cp diets with a constant energy:protein ratio. Although much work has been conducted on reducing the CP and ME content of broiler diets in open-type houses using local nutrient requirements for subtropical region, very little experimentation has been done in environmentally controlled houses using nutrient recommendations for the Hubbard strain. Therefore, the present study was planned to determine whether a low-cp diet with a constant ME:CP ratio can support growth performance and 468

2 LOW-PROTEIN DIETS WITH CONSTANT ENERGY-TO-PROTEIN RATIO 469 Table 1. Ingredient and nutrient composition of broiler starter diets containing low protein with constant energy:protein ratio (1 to 10 d) Ingredient A B C D (%) Corn Rice polishings Wheat bran 8.41 Canola meal Guar meal Soybean meal Fish meal 60% Limestone Dicalcium phosphate L-Lys HCl DL-Met L-Thr Sodium chloride Sodium bicarbonate Vegetable oil Vitamin-mineral premix Total Nutrient composition (%) ME, kcal/kg 3,036 2,904 2,772 2,640 CP Energy:protein ratio Crude fiber Ether extract Ca Available P Lys Met Cystine Thr Trp Supplied the following per kilogram of diet: vitamin A (as retinyl acetate), 14,000 IU; vitamin D 3 (as cholecalciferol), 3,500 IU; vitamin K (menadione sodium bisulfite), 2.8 mg; vitamin E (as D-α-tocopherol), 42 IU; biotin, 0.07 mg; folic acid, 1.7 mg; niacin, 35 mg; calcium pantothenate, 12.3 mg; pyridoxine, 3.4 mg; riboflavin, 7 mg; thiamin, 1.7 mg; vitamin B 12, 12.1 g; Fe, 98 mg; Mn, 112 mg; Cu, 9.8 mg; Se, 0.07 mg; Zn, 70 mg; choline chloride, 550 mg; salinomycin (as Phibro coccidiostat), 60 mg; and zinc bacitracin (as Albac 10%), 50 mg. 2 Digestible. carcass characteristics of broilers equal to that of a high- CP diet from 1 to 35 d of age. MATERIALS AND METHODS All methods and management procedures used in this study were in compliance with the guidelines established by the Institutional Animal Care and Use Committee, University of Agriculture, Faisalabad, Pakistan. Birds and Housing The experiment was conducted in an environmentally controlled house. A total of 1,760 one-day-old straightrun Hubbard broiler chickens were randomly divided into 16 experimental units of 110 chickens each and allotted randomly to different experimental treatments. Birds were vaccinated for Newcastle disease virus on d 6 and 24, for hydropericardium syndrome on d 15, and for Gumboro disease on d 10 and 20. The birds were kept under standard management conditions, and feed and water were provided ad libitum throughout the experimental period. The whole experimental period was divided into 3 phases: starter (1 to 10 d), grower (11 to 26 d), and finisher (27 to 35 d) according to the Hubbard (2004) management guide. Experimental Diets The feed ingredients used for the formulation of experimental diets were analyzed in triplicate for their DM (method number ), CP (method number ), ether extract (method number ), crude fiber (method number ; AOAC, 1990), and AA contents (Degussa AG, Dusseldorf, Germany). The N content was analyzed in triplicate by the Kjeldahl procedure, and CP was calculated as N The fat content was determined in triplicate as ether extract using a Soxhlet apparatus. Nutrient recommendations for the Hubbard strain were used as control, because this strain is mostly reared in the country. The ME:CP ratio was maintained at 132, 143, and 155 in starter, grower, and finisher diets, respectively. Four experimental diets were formulated to have 4 levels of CP and ME, respectively, in each phase: 23, 22, 21, and 20% CP with 3,036, 2,904, 2,772, and 2,640 kcal/kg in the starter phase; 22, 21, 20, and 19% CP with 3,146, 3,003, 2,860, and 2,717 kcal/kg in the grower phase; and 20, 19, 18, and 17% CP with 3,100, 2,945, 2,790, and

3 470 KAMRAN ET AL. Table 2. Ingredient and nutrient composition of broiler grower diets containing low protein with constant energy:protein ratio (11 to 26 d) Ingredient A B C D (%) Corn Rice polishings Wheat bran 6.90 Canola meal Guar meal Soybean meal Fish meal 60% Limestone Dicalcium phosphate L-Lys HCl DL-Met L-Thr Sodium chloride Sodium bicarbonate Vegetable oil Vitamin-mineral premix Total Nutrient composition (%) ME, kcal/kg 3,146 3,003 2,860 2,717 CP Energy:protein ratio Crude fiber Ether extract Ca Available P Lys Met Cystine Thr Trp Supplied the following per kilogram of diet: vitamin A (as retinyl acetate), 14,000 IU; vitamin D 3 (as cholecalciferol), 3,500 IU; vitamin K (menadione sodium bisulfite), 2.8 mg; vitamin E (as D-α-tocopherol), 42 IU; biotin, 0.07 mg; folic acid, 1.7 mg; niacin, 35 mg; calcium pantothenate, 12.3 mg; pyridoxine, 3.4 mg; riboflavin, 7 mg; thiamin, 1.7 mg; vitamin B 12, 12.1 g; Fe, 98 mg; Mn, 112 mg; Cu, 9.8 mg; Se, 0.07 mg; Zn, 70 mg; choline chloride, 550 mg; salinomycin (as Phibro coccidiostat), 60 mg; and zinc bacitracin (as Albac 10%), 50 mg. 2 Digestible. 2,635 kcal/kg in the finisher phase. Digestible Lys was maintained at 1.10, 1.02, and 0.90% of the diet in the starter, grower, and finisher periods, respectively, and remaining limiting AA like Met, Thr, and Trp were included according to Hubbard recommendations. The nutrient composition of the diets either met or exceeded the Hubbard recommendations for broiler diets, except CP and ME, which were reduced in other diets maintaining a constant ME:CP ratio (Tables 1, 2, and 3). Analysis of diets for CP and AA concentration matched closely with the calculated values. Each experimental diet was offered randomly to 4 replicates, and the experimental diets were fed up to 35 d of age. Data Collection Feed intake and weight gain were recorded at the end of each phase, and feed conversion ratio (FCR) was calculated using these data. Protein efficiency ratio (PER) and energy efficiency ratio (EER) were also calculated for each phase. The PER was calculated as grams of weight gain per gram of protein intake, whereas the EER was calculated as grams of weight gain 100/total ME intake. At the end of experiment, 5 birds from each replicate (with no visible abnormalities) were randomly selected and slaughtered, and data on carcass yield (including skin and giblets and calculated as % of live weight), deboned breast meat yield, thigh yield, abdominal fat, and relative weights of liver and heart (calculated as % of carcass weight with giblets) were recorded. A record of mortality of experimental birds was also maintained during the entire experiment. Statistical Analysis The results were analyzed by GLM, and Tukey s significant difference test was used to compare means (Minitab 13.1, Minitab Inc., State College, PA). Linear and quadratic regression analyses were also done to estimate the response of birds to various dietary treatments (Steel et al., 1997). RESULTS AND DISCUSSION There were significant differences (P < 0.05) in weight gain, feed intake, and FCR among dietary treatments during grower, finisher, and overall experimental periods. Weight gain was linearly decreased, whereas feed intake and FCR were increased (P < 0.05) linearly with the reduction in dietary CP and ME levels during these periods.

4 LOW-PROTEIN DIETS WITH CONSTANT ENERGY-TO-PROTEIN RATIO 471 Table 3. Ingredient and nutrient composition of broiler finisher diets containing low protein with constant energy:protein ratio (27 to 35 d) Ingredient A B C D (%) Corn Rice polishings Wheat bran Canola meal Guar meal Sunflower meal 6.00 Soybean meal Fish meal 60% Limestone Dicalcium phosphate L-Lys HCl DL-Met L-Thr Sodium chloride Sodium bicarbonate Vegetable oil Vitamin-mineral premix Total Nutrient composition (%) ME, kcal/kg 3,100 2,945 2,790 2,635 CP Energy:protein ratio Crude fiber Ether extract Ca Available P Lys Met Cystine Thr Trp Supplied the following per kilogram of diet: vitamin A (as retinyl acetate), 14,000 IU; vitamin D 3 (as cholecalciferol), 3,500 IU; vitamin K (menadione sodium bisulfite), 2.8 mg; vitamin E (as D-α-tocopherol), 42 IU; biotin, 0.07 mg; folic acid, 1.7 mg; niacin, 35 mg; calcium pantothenate, 12.3 mg; pyridoxine, 3.4 mg; riboflavin, 7 mg; thiamin, 1.7 mg; vitamin B 12, 12.1 g; Fe, 98 mg; Mn, 112 mg; Cu, 9.8 mg; Se, 0.07 mg; Zn, 70 mg; choline chloride, 550 mg; salinomycin (as Phibro coccidiostat), 60 mg; and zinc bacitracin (as Albac 10%), 50 mg. 2 Digestible. However, these parameters were unaffected during the starter period (Table 4). The PER and EER were decreased (P < 0.05) linearly during grower, finisher, and overall period, whereas no difference was observed during the starter period (Table 5). Mortality was not significantly different among treatments (Table 5). Similarly, carcass characteristics like carcass yield, breast meat yield, thigh yield, abdominal fat, and relative weights of liver and heart were also unaffected by the reduction in dietary CP content with constant ME:CP ratio. Growth Performance Feed intake was linearly increased with reduced CP and ME diets during grower, finisher, and overall periods. This observation was in agreement with reports by Golian and Maurice (1992) and Leeson et al. (1993), who reported that birds consume feed to primarily meet their energy requirements. Morris (1968) also suggested that the effect of dietary energy on the performance of growing birds is dependent on the capacity of the bird to alter feed intake to meet changing demands for calories. The feed intake during the starter period remained unchanged. In the starter period, birds might have had a physical limitation when trying to consume the low-density diets due to which feed intake was not altered during this period. This finding was in agreement with Griffiths et al. (1977), who suggested that a reduction in energy intake is due to physical limitations, because birds cannot eat more to compensate for reduced energy density of the diet during early age. As the birds become larger, the physical constraint on the amount of feed intake is decreased. These results were supported by the findings of Hidalgo et al. (2004), who found that birds fed the lowest dietary regimen with a constant ME:CP ratio had increased their feed intake during the finisher and overall experimental period, whereas it was unaffected during the starter period. Weight gain and FCR were severely depressed during all the growth periods except the starter period. During the starter period, the trend was the same; however, the difference was nonsignificant. The birds provided low- CP and low-me diets had increased feed consumption, but this increase could not compensate for the reduced growth and did not allow for complete recovery of final BW. The difference in rate and efficiency of growth probably occurred due to poor efficiency of utilization of ME and CP, although critical AA were according to the re-

5 472 KAMRAN ET AL. Table 4. Growth performance of broilers fed different diets containing low protein with constant energy:protein ratio 1 Weight gain (g/bird) Feed intake (g/bird) Feed conversion ratio (g:g) Starter Grower Finisher Overall Starter Grower Finisher Overall Starter Grower Finisher Overall Item (1 to 10 d) (11 to 26 d) (27 to 35 d) (1 to 35 d) (1 to 10 d) (11 to 26 d) (27 to 35 d) (1 to 35 d) (1 to 10 d) (11 to 26 d) (27 to 35 d) (1 to 35 d) Diets 2 A ab a 1,642.8 a ,482.2 c 1,476.5 c 3,233.4 b b 2.10 d 1.97 d B a b 1,615.4 a ,515.0 bc 1,598.1 bc 3,385.8 b b 2.42 c 2.10 c C bc b 1,520.4 b ,578.2 ab 1,720.9 ab 3,578.7 a a 2.68 b 2.35 b D c c 1,470.3 b ,645.2 a 1,816.1 a 3,738.5 a a 2.97 a 2.54 a SEM ANOVA Probability Diet <0.001 < <0.001 <0.001 < <0.001 <0.001 <0.001 Linear <0.001 < <0.001 <0.001 < <0.001 <0.001 <0.001 Quadratic a d Means within a column with different superscripts differ significantly (P < 0.05). 1 Means of 4 replicates with 110 birds in each replicate. 2 Diet A contained 23, 22, and 20% CP and 3,036, 3,146, and 3,100 kcal/kg of ME; diet B contained 22, 21, and 19% CP and 2,904, 3,003, and 2,945 kcal/kg of ME; diet C contained 21, 20, and 18% CP and 2,772, 2,860, and 2,790 kcal/kg of ME; and diet D contained 20, 19, and 17% CP and 2,640, 2,717, and 2,635 kcal/kg of ME for starter, grower, and finisher periods, respectively. quirements. This might be due to inadequate levels of 1 or more lesser-essential AA like Arg, Ile, and Val in the low-cp diets, because levels of these AA were not taken care, and these lesser-essential AA can be a limiting factor when CP is reduced. Hidalgo et al. (2004) also found that weight gain and FCR were adversely affected when the broilers were fed diets formulated to contain suboptimum concentrations of CP and ME. Providing a diet containing a suboptimal concentration of ME may have a more pronounced effect on performance with broilers marketed at lighter weights, because the duration of the production period does not allow for compensatory growth as with heavy broilers marketed at older ages. Sizemore and Siegel (1993) compared different ME and CP concentrations while maintaining a constant ME:CP ratio. It was observed that birds receiving the lower-density starter diets were significantly lighter than those fed the higher density diets at 3 wk of age, whereas at 7 wk of age, no treatment differences in BW were apparent. The PER and EER were decreased linearly during the grower, finisher, and overall experimental period as a result of lowering the dietary CP and ME content. The PER and EER during the starter period were unaffected with the reduction in dietary CP and ME content. Although the birds fed on low-cp and low-me diets consumed the same amount of protein and energy due to increased feed intake, there was a significant depression in weight gain of the birds. As a result, the PER and EER were decreased with reduced CP and ME diets. The results regarding PER were not supported by the findings of Cheng et al. (1997b), who observed a linear increase in PER with the reduction in dietary CP content from 24 to 16%. However, the main difference in their study was the constant energy level across all the dietary treatments. However, the results regarding EER were consistent with the findings of Cheng et al. (1997a), who observed that EER was decreased with low-me diets. No significant differences in mortality occurred due to dietary treatments. Carcass Characteristics The experiment averages for carcass yield, deboned breast meat yield, thigh yield, abdominal fat, liver weight, and heart weight were 63.8, 21.9, 14.3, 2.52, 4.24, and 0.92%, respectively (data not shown). Dietary treatments did not alter the yield of carcass or the amount of its associated abdominal fat. Similarly, there was no difference in deboned breast meat yield, thigh yield, and liver and heart weights due to different dietary treatments. It may be mentioned that perhaps the carcass yield and breast meat yield were not affected due to adequate levels of essential AA, particularly Lys and Met, in low-cp diets, because these 2 AA are exclusively used for protein accretion in the body (Si et al., 2001; Baker et al., 2002). As a consequence of enhanced de novo lipogenesis in the liver of birds fed the low-cp diets (Rosebrough and Steele, 1985; Swennen et al., 2006), birds are expected to have increased liver weights and deposit more abdominal fat

6 LOW-PROTEIN DIETS WITH CONSTANT ENERGY-TO-PROTEIN RATIO 473 Table 5. Overall mortality, protein efficiency ratio, and energy efficiency ratio of broilers fed different diets containing low protein with constant energy:protein ratio 1 Protein efficiency ratio 2 (g:g) Energy efficiency ratio 3 (%) Mortality (%) Starter Grower Finisher Overall Starter Grower Finisher Overall Overall Item (1 to 10) (11 to 26) (27 to 35) (1 to 35) (1 to 10) (11 to 26) (27 to 35) (1 to 35) (1 to 35) Diets 4 A ab 2.38 a 2.40 a ab a a 6.14 B a 2.18 b 2.37 a a b a 7.27 C b 2.07 bc 2.22 b b bc b 4.09 D b 1.98 c 2.17 b b c b 4.32 SEM ANOVA Probability Diet <0.001 < <0.001 < Linear <0.001 < <0.001 < Quadratic a c Means within a column with different superscripts differ significantly (P < 0.05). 1 Means of 4 replicates with 110 birds in each replicate. 2 Calculated as weight gain divided by protein intake. 3 Calculated as weight gain 100/total ME intake. 4 Diet A contained 23, 22, and 20% CP and 3,036, 3,146, and 3,100 kcal/kg of ME; diet B contained 22, 21, and 19% CP and 2,904, 3,003, and 2,945 kcal/kg of ME; diet C contained 21, 20, and 18% CP and 2,772, 2,860, and 2,790 kcal/kg of ME; and diet D contained 20, 19, and 17% CP and 2,640, 2,717, and 2,635 kcal/kg of ME for starter, grower, and finisher periods, respectively. due to increased ME:CP ratio. However, in the present study, it was not the case, and liver weights and abdominal fat remained nonsignificant among the dietary treatments. This might be due to a constant ME:CP ratio that was maintained across all the dietary treatments. Hidalgo et al. (2004) also reported no differences in carcass yield, breast meat yield, and abdominal fat pad in broilers fed low-cp diets with a constant ME:CP ratio. However, Dozier and Moran (2001, 2002) reported that feeding broiler diets formulated to contain suboptimum concentrations of CP and ME impaired the amount and yield of carcass parts. In conclusion, feeding broiler chickens diets containing low CP with a constant ME:CP ratio has adversely affected the growth performance even when standard levels of critical AA were maintained in the diets. However, carcass parameters were unaltered without any increase in abdominal fat content. In general, the optimum performance in the present experiment was obtained by broilers fed diets formulated to contain 23, 22, and 20% CP and 3,036, 3,146, and 3,100 kcal/kg of ME for starter, grower, and finisher periods, respectively. ACKNOWLEDGMENTS We gratefully acknowledge the support of Muhammad Aslam, Islamabad Feeds and Chicks, Rawalpindi, Pakistan, who provided the chickens, feed, and experimental and lab facilities at its research and development farm for the present trial. REFERENCES Aletor, V. A., I. I. Hamid, E. Niess, and E. Pfeffer Low protein amino acids supplemented diets in broiler chickens: Effects on performance, carcass characteristics, whole body composition and efficiencies of nutrient utilization. J. Sci. Food Agric. 80: AOAC Official Methods of Analysis. 16th ed. Assoc. Offic. Anal. Chem., Arlington, VA. Baker, D. H., A. B. Batal, T. M. Parr, N. R. Augspurger, and C. M. 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