Effects of the dietary level and source of sodium on growth performance, gastrointestinal digestion and meat characteristics in turkeys

Animal Feed Science and Technology 178 (2012) 74–83

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Effects of the dietary level and source of sodium on growth performance, gastrointestinal digestion and meat characteristics in turkeys b ´ J. Jankowski a , J. Ju´skiewicz b,∗ , K. Lichtorowicz a , Z. Zdunczyk a b

Department of Poultry Science, University of Warmia and Mazury in Olsztyn, 5 Oczapowskiego Street, 10-718 Olsztyn, Poland Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, 10 Tuwima Street, 10-748 Olsztyn, Poland

a r t i c l e

i n f o

Article history: Received 20 March 2012 Received in revised form 28 September 2012 Accepted 28 September 2012

Keywords: Dietary Na salt Blood electrolyte Intestine Meat Growth Turkey

a b s t r a c t The aim of this 18 wk study was to evaluate whether a substantial decrease in dietary Na content and the use of Na sources alternative to NaCl might affect the growth performance, gastrointestinal digestion processes, carcass and breast meat traits of male turkeys. A total of 630 one-day-old heavy-type Large White BIG-6 male turkeys were assigned to nine dietary treatments according to a 3 × 3 factorial completely randomized design. The experimental factors included increasing supplementation levels of Na (0.8, 1.3, 1.8 g/kg) added to a basal diet containing 0.15–0.24 g Na/kg, and different Na sources (NaCl, NaHCO3 , Na2 SO4 ). Regarding the gastrointestinal, carcass and meat parameters only two levels of Na supplementation (0.8, 1.8 g/kg) were evaluated. Increasing Na supplementation increased the growth rate of birds during wk 0–12 of the experiment, and the feed conversion ratio in particular over the first 4 wk (P<0.05, 0.8 vs. 1.3 and 1.8 g/kg). Sodium sources affected (P<0.05) feed conversion in particular during wk 9–12 of feeding, which was reflected in a decreased feed conversion rate in the NaHCO3 and Na2 SO4 treatments, compared with the NaCl treatment. The foot pad dermatitis score was not affected (P>0.05) by Na levels or sources. Sodium levels did not change (P>0.05) gastrointestinal parameters (i.e. pH, dry matter concentration), but they reduced (P<0.05, 0.8 vs. 1.8 g/kg) the serum concentrations of Mg, P, Na, and Cl. Sodium sources affected (P<0.05) gastrointestinal parameters. NaHCO3 supplementation increased viscosity and dry matter concentrations in the small intestine, compared with the NaCl treatment, whereas Na2 SO4 increased caecal dry matter concentrations. The activity levels of ␤-glucosidase and ␤-glucuronidase in the caeca were affected (P<0.05) by the Na source, caecal enzyme activities were increased by NaHCO3 , in comparison with NaCl and Na2 SO4 supplementation. Short-chain fatty acid concentrations were not affected by Na levels or sources in the diet, except for acetate whose content increased with increasing Na levels (0.8 vs. 1.8 g/kg) and iso-butyrate which was affected (P<0.05) by Na source (NaHCO3 vs. Na2 SO4 and NaCl). Carcass and meat traits were partly affected (P<0.05) © 2012 Elsevier B.V. All rights reserved.

Abbreviations: a*, redness; b*, yellowness; BW, body weight; BWG, body weight gain; Ca, calcium; Cl, chloride; D, dosage effect; DEB, dietary electrolyte balance; DM, dry matter; FCR, feed conversion ratio; FPD, foot pad dermatitis; H2 SO4 , sulphuric acid; K, potassium; L*, lightness; Mg, magnesium; Na, sodium; NaCl, sodium chloride; NaHCO3 , sodium bicarbonate; Na2 SO4 , sodium sulphate; P, phosphorus; PSE, pale soft exudative meat; S, salt effect; SD, standard deviation; SCFA, short-chain fatty acid; SEM, standard error of the mean. ∗ Corresponding author. Tel.: +48 89 523 46 73; fax: +48 89 524 01 24. E-mail address: [email protected] (J. Ju´skiewicz). 0377-8401/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.anifeedsci.2012.09.012

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by Na source, NaCl supplementation increased breast yield in comparison with NaHCO3 , and it decreased L* values, compared with NaHCO3 and Na2 SO4 supplementation. Our findings show that a Na deficiency in the diet (0.8 g/kg) decreases the growth rate of turkeys and reduces the efficiency of feed utilisation. Sodium sources alternative to NaCl improve feed utilisation, but they may adversely affect breast muscle traits. © 2012 Elsevier B.V. All rights reserved.

1. Introduction The negative consequences of an increased dietary intake of Na include higher water consumption levels and a higher moisture content of litter (Mushtaq et al., 2007) which may increase the risk of many diseases and other health problems encountered in poultry production (Francesch and Brufau, 2004). A review of the recent literature shows that studies addressing the above issues have been conducted primarily on broiler chickens, while the number of experiments involving turkeys remains low. Thus, extensive research on the latter species has been postulated (Jankowski et al., 2011a). According to the National Research Council (1994), the minimum Na, K and Cl requirements of growing turkeys are 1.7, 7.0 and 1.5 g/kg diet, respectively, corresponding to a dietary electrolyte balance (DEB) of 211 mEq/kg. A linear relationship between Na consumption and the moisture content of excreta was observed in broilers fed diets characterised by a wide range (207–300 mEq/kg) of DEB values (Borges et al., 2003; Mushtaq et al., 2007). Therefore, a dietary application of NaCl, a common salt used as a feed ingredient, is an important consideration due to the reported increased excreta moisture associated with an elevated dietary Na and Cl content (Jankowski et al., 2011b). An adequate Na intake seems to be essential in numerous physiological processes, it affects enzyme activity and tissue protein synthesis (Olanrewaju et al., 2007). Some authors reported a beneficial influence of an increased dietary Na level on feed consumption, and thus the growth rate of broilers (Watkins et al., 2005; Mushtaq et al., 2007). Other researchers recommended a lower NaCl dosage (GfE, 1999) for broilers linking a higher moisture content of litter with an increased risk of many diseases, including foot pad dermatitis (FPD). Therefore, efforts have been made to use other sources of Na in poultry nutrition (Mushtaq et al., 2007; Jankowski et al., 2011b). Recent work on broilers revealed that Na2 SO4 , compared with NaHCO3 , seems to be a better alternative to dietary NaCl–especially during the starter period, as manifested by better feed utilisation, lower excreta moisture, and a lower FPD score (Jankowski et al., 2011b). On the other hand, very little information is available on the usefulness of NaCl alternatives in turkey nutrition, thus these issues should be more thoroughly investigated. In view of the above dietary concerns, this study was undertaken to evaluate the effect of different dietary Na levels (0.8, 1.3, 1.8 g/kg) and Na sources (NaCl, NaHCO3 , Na2 SO4 ) on growth performance, feed conversion, small intestinal parameters (pH, viscosity, dry matter concentration), caecal fermentation processes (bulk effect, pH, microbial enzyme activity, short-chain fatty acid production), and breast meat quality characteristics (pH, colour indices) in turkeys. 2. Materials and methods 2.1. Animal protocol and dietary treatments The animal protocol used in this study was approved by the Local Institutional Animal Care and Use Committee, and the study was carried out in accordance with EU Directive 2010/63/EU for animal experiments (OJEU, 2010). An 18 wk experiment was conducted at the Research Laboratory of the Department of Poultry Science, University of Warmia and Mazury in Olsztyn. A total of 630 one-day-old heavy-type Large White BIG-6 male turkeys, sexed at a local commercial hatchery (Ketrzyn, Poland), were randomly assigned to nine groups comprised of seven replicates, each of ten birds. The turkeys were kept in pens (4 m2 each) on litter (wood shavings) in a building with a strictly controlled environment. Light was provided for 16 h per d. Indoor temperature was 32 ◦ C at the beginning of the experiment and 16 ◦ C at the end of wk 18. The birds had free access to feed and water. A 3 × 3 factorial design of 9 dietary treatments was used to evaluate the effects of graded levels of dietary Na (0.8, 1.3 and 1.8 g/kg) and different Na sources (NaCl, NaHCO3 and Na2 SO4 ). The composition of the basal diet is given in Table 1. The dietary Na levels were accomplished with the use of different premixes containing one of Na sources (Table 2). The premix, different for each diet, was mixed with the basal diet (1:99 w/w). Diets were assayed for the content of Na and K using flame atomic absorption spectroscopy. Dietary Cl content was determined by the biamperometric technique. The DEB was calculated using the formula: DEB mEq/kg = Na mEq/kg + K mEq/kg − Cl mEq/kg (Mongin, 1981). The carcass dressing percentage was calculated after 24 h chilling using the following formula: carcass weight including neck, relative to live body weight (in g/kg). 2.2. Measurements At the end of each feeding period, on d 28, 56, 84, and 126 of the experiment, the birds were weighed, and feed intake was recorded. Body weight gain (BWG) and feed conversion ratio (FCR) were calculated for each period. The excreta dry matter (DM) was estimated on d 49 and 112. Mortality rates were recorded daily, and the weights of dead birds were used to adjust average daily gain, average daily feed intake, and FCR. For performance indices, each replicate (n = 7) was considered as the

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J. Jankowski et al. / Animal Feed Science and Technology 178 (2012) 74–83

Table 1 Dietary ingredients and the nutrient content of the basal diet (g/kg on an as fed basis unless otherwise stated)a . Feeding period (wk) 0–4

5–8

9–12

13–18

Wheat Maize Triticale Soya bean meal (460 g crude protein/kg) Rapeseed (207 g crude protein/kg) Potato protein (750 g crude protein/kg) Soybean oil Lard Limestone Monocalcium phosphate l-Lysine HCl (780 g lysine/kg)b DL-Methionine (990 g methionine/kg)c l-Threonine (985 g threonine/kg)b Premixd

307.4 150.0 – 400.6 40.0 40.0 13.3 – 16.6 21.7 3.20 2.20 – 5.00

401.3 127.5 – 340.3 34.0 34.0 21.3 – 14.1 18.5 2.70 1.60 – 4.70

612.5 – 50.0 232.8 60.0 – 11.5 – 16.0 6.50 4.20 1.00 1.30 4.00

662.5 – 50.0 164.6 60.0 – – 28.8 15.1 9.90 4.20 0. 70 0. 60 3.50

Calculated nutrient compositione Metabolisable energy (MJ/kg) Crude protein Lysine Methionine Methionine + cysteine Threonine Tryptophan Ca Available P Na Cl

11.9 280.6 17.5 6.40 11.2 10.6 3.50 12.5 6.40 0.24 0.91

12.1 257.6 15.4 5.90 10.4 9.60 3.30 10.7 5.80 0.22 0.84

12.6 215.0 12.8 4.30 8.50 8.50 2.70 9.00 3.30 0.17 0.72

13.2 190.0 11.2 3.60 7.60 6.80 2.40 9.00 4.00 0.15 0.70

a In the experimental treatments, Na was added in the amount of 0.8, 1.3 and 1.8 g/kg of a diet. Dietary Na levels were reached with the use of a premix containing experimental Na salts (NaCl, or NaHCO3 , or Na2 SO4 ). The premix, different for each diet, was mixed with the basal fodder (1:99 w/w). b Ajinomoto Eurolysine S.A.S, Amiens, France. c MetAMINO® , Evonik Degussa Gmbh, Essen, Germany. d Provided the following per kilogram of diet in the successive (0–4, 5–8, 9–12, and 13–18 wk) feeding periods: retinol 3.60, 3.38, 2.88, and 2.52 mg, cholecalciferol 0.13, 0.12, 0.10, and 0.09 mg, ␣-tocopheryl acetate 100, 94, 80, and 70 mg, vitamin K3 6.0, 5.6, 4.8, and 4.2 mg, thiamine 5.0, 4.7, 4.0, and 3.5 mg, riboflavin 8.0, 7.5, 6.4, and 5.6 mg, pyridoxine 6.0, 5.6, 4.8, and 4.2 mg, cobalamin 0.030, 0.028, 0.024, and 0.021 mg, biotin 0.30, 0.28, 0.24, and 0.21 mg, pantothenic acid 25, 24, 20, 18 mg, nicotinic acid 80, 75, 64, and 56 mg, folic acid 3.0, 2.8, 2.4, and 2.1 mg, Fe 60, 56, 48, and 42 mg, Mn 120, 112, 96, and 84 mg, Zn 110, 103, 88, and 77 mg, Cu 20, 19, 16, and 14 mg, J 3.0, 2.8, 2.4, and 2.1 mg, Se 0.30, 0.28, 0.24, and 0.21 mg, choline chloride 400, 376, 320, and 280 mg, respectively. e Calculated from the analyses of feed ingredients provided by the manufacturer.

experimental unit. On d 55 and 125, the incidence and severity of FPD were assessed based on the scoring system developed by Hocking et al. (2008). Due to the similar growth performance of the experimental groups receiving medium (1.3 g/kg) and high (1.8 g/kg) Na levels, and to reduce overall expenses, gastrointestinal, carcass and meat traits of the experimental groups receiving 0.8 and 1.8 g/kg Na supplementation levels were further evaluated. At the end of the trial, seven turkeys representing an average body weight of each group were selected, tagged, and fasted for 8 h. Blood samples were collected from the wing vein. Serum samples were prepared by solidification and low-speed centrifugation at 300 × g for 10 min at 4 ◦ C. Serum analyses were performed using the COBAS INTEGRA 400 Plus system (Roche, Meylan, France). The concentrations of Ca, P, Mg, urea, uric acid, and creatinine were determined by the colorimetric methods, and the levels of Na, K, and Cl by indirect potentiometry. The birds were killed by cervical dislocation after electrical stunning, scalded, defeathered, and eviscerated. Abdominal fat weight was measured. The jejunum, ileum, and caeca were removed and weighed with the contents. The jejunal, ileal, and caecal pH was measured directly in the intestine using a microelectrode and a pH/ION meter (model 301, Hanna Instruments, Vila do Conde, Portugal). Samples of the jejunal, ileal and caecal contents were stripped carefully from the intestine and used for immediate analyses, i.e. ammonia, DM, viscosity, short-chain fatty acids (SCFA). The remaining of the caecal digesta was transferred to tubes and stored at −70 ◦ C. The caeca were flushed with water, blotted on filter paper and weighed as the tissue mass. Digesta DM was determined at 105 ◦ C. Small intestinal digesta samples were mixed on a vortex, and centrifuged at 10,000 × g for 10 min. The 0.5 mL supernatant fraction was placed in a Brookfield LVDV-II + cone-plate rotational viscometer (CP40; Brookfield Engineering Laboratories Inc., Stoughton, MA, USA) and viscosity was measured at 39 ◦ C and at a shear rate of 60 per minute. In fresh caecal digesta, ammonia was extracted, trapped in a solution of boric acid in Conway’s dishes, and determined by direct titration with H2 SO4 . Short-chain fatty acids were analysed using Shimadzu GC-2010 (Kyoto, Japan) equipped with a capillary column SGE BP21, 30 m × 0.53 mm (SGE Europe Ltd., Kiln Farm Milton Keynes, UK) as described previously (Ju´skiewicz et al., 2006). The activity of bacterial enzymes, ␣- and ␤-glucosidase, ␣- and ␤-galactosidase and

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Table 2 Na, K, Cl content (g/kg) and dietary electrolyte balance (DEB, mEq/kg) in experimental diets. Na addition

Na sourcea

Salt addition

wk

Nab

Kb

Clb

DEBc

1.8 g/kg

NaCl

4.57 g/kg

NaHCO3

6.58 g/kg

Na2 SO4

5.56 g/kg

0–4 5–8 9–12 13–18 0–4 5–8 9–12 13–18 0–4 5–8 9–12 13–18

1.66 1.75 1.92 1.84 1.58 1.67 1.63 1.72 1.67 1.70 1.75 1.82

11.32 9.54 8.40 7.26 11.32 9.54 8.40 7.26 11.32 9.54 8.40 7.26

3.9 3.7 4.4 4.2 1.4 1.5 1.6 1.6 1.4 1.3 1.6 1.4

252 216 174 147 319 274 241 215 323 281 246 225

NaCl

3.30 g/kg

NaHCO3

4.75 g/kg

Na2 SO4

4.02 g/kg

0–4 5–8 9–12 13–18 0–4 5–8 9–12 13–18 0–4 5–8 9–12 13–18

1.26 1.28 1.34 1.40 1.22 1.25 1.32 1.31 1.29 1.29 1.27 1.32

11.32 9.54 8.40 7.26 11.32 9.54 8.40 7.26 11.32 9.54 8.40 7.26

3.3 2.9 3.4 3.3 1.5 1.5 1.7 1.5 1.5 1.3 1.5 1.6

251 218 177 154 300 256 224 200 303 264 228 198

NaCl

2.03 g/kg

NaHCO3

2.93 g/kg

Na2 SO4

2.47 g/kg

0–4 5–8 9–12 13–18 0–4 5–8 9–12 13–18 0–4 5–8 9–12 13–18

0.88 0.88 0.93 0.84 0.83 0.99 0.81 0.81 0.81 0.92 0.86 0.85

11.32 9.54 8.40 7.26 11.32 9.54 8.40 7.26 11.32 9.54 8.40 7.26

2.7 2.5 2.7 2.7 1.6 1.8 1.6 1.4 1.6 1.4 1.5 1.6

252 212 179 146 280 236 205 181 279 244 210 178

1.3 g/kg

0.8 g/kg

a b c

NaCl (393.4 g Na/kg), NaHCO3 (273.8 g Na/kg), Na2 SO4 (323.9 g Na/kg). Analyzed content of minerals. DEB (mEq/kg) = Na mEq/kg + K mEq/kg − Cl mEq/kg (Mongin, 1981).

␤-glucuronidase, was measured by the rate of p- or o-nitrophenol release from their nitrophenylglucosides (Ju´skiewicz and ´ Zdunczyk, 2002). The carcasses were chilled in an aerated chill tank for 30 min, removed, and allowed to drain. After slaughter, breast, thigh and shank muscles were dissected from each carcass and were cooled at 4 ◦ C. After carcass measurements had been performed, skinless breast meat samples were weighed and collected to determine muscle characteristics. Meat (breast muscles) pH was measured at 15 min, 1 and 24 h after carcass chilling (pH-meter, Testo 206–pH2 model, Testo AG, Lenzkirch, Germany). Hunter L* (lightness, lower values indicate a darker colour), a* (redness, higher positive values indicate a higher contribution of redness), and b* (yellowness, higher values indicate a higher contribution of yellowness) values were determined on breast muscle samples using a MiniScan XE Plus colour difference meter (Hunter Associates Laboratory Inc., Reston, VA, USA). The average of three readings taken from the cross-section of the muscle free from colour defects, bruising and haemorrhages was recorded.

2.3. Statistics The data were analysed using the STATISTICA software package version 8.0 (StatSoft Corp., Krakow, Poland). A two-way repeated measures ANOVA was applied to assess the effects of main factors: sodium level (D), sodium source (S) and their interaction (D × S). If the analysis revealed a significant interaction or that both dietary factors had a significant influence, the differences among the individual groups were then analysed using Tukey’s multiple range post hoc test. Data had been checked for normality before the statistical analysis was performed. Differences were considered to be significant at P≤0.05. The pooled SEM was calculated as the standard deviations from all measurements divided by their square root.

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J. Jankowski et al. / Animal Feed Science and Technology 178 (2012) 74–83

Table 3 Final body weight (BW), body weight gain (BWG), feed conversion ratio (FCR) in turkeys fed diets with different Na salts. Additional Na/source

NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 SEMa

1.8 g/kg

1.3 g/kg

0.8 g/kg

BW (kg)

BWG (kg)

FCR (kg/kg)

wk 18

wk 0–4

wk 5–8

wk 9–12

wk 13–18

wk 0–4

wk 5–8

wk 9–12

wk 13–18

17.61 17.88 18.05 17.66 18.14 18.15 17.33 17.62 17.40 0.077

1.16 1.07 1.09 1.18 1.10 1.10 1.01 0.97 0.90 0.013

3.49 3.53 3.58 3.63 3.58 3.54 3.36 3.42 3.27 0.026

5.80 5.76 5.94 5.62 5.93 5.82 5.61 5.68 5.69 0.027

7.09 7.47 7.38 7.16 7.47 7.62 7.30 7.49 7.48 0.057

1.52yz 1.56y 1.54yz 1.46z 1.56y 1.50yz 1.77x 1.68x 1.72x 0.016

1.86y 1.81yz 1.84yz 1.80yz 1.75z 1.81yz 1.99x 1.78yz 1.79yz 0.013

2.29 2.20 2.20 2.27 2.20 2.16 2.34 2.27 2.21 0.015

3.91 3.88 3.70 3.69 3.85 3.61 3.67 3.66 3.61 0.036

Dosage effect (D)

1.8 g/kg 1.3 g/kg 0.8 g/kg

17.85x 17.98x 17.45y

1.11x 1.133x 0.96y

3.53x 3.58x 3.35y

5.84x 5.79x 5.66y

7.31 7.41 7.42

1.54y 1.51y 1.72x

1.84xy 1.79y 1.85x

2.23 2.21 2.28

3.83 3.72 3.65

Salt effect (S)

NaCl NaHCO3 Na2 SO4

17.53 17.88 17.87

1.12x 1.05y 1.03y

3.50 3.51 3.46

5.68 5.79 5.82

7.18y 7.47x 7.49x

1.58 1.60 1.59

1.89x 1.78y 1.81y

2.30x 2.23y 2.19y

3.76 3.80 3.64

<0.001 <0.001 0.364

<0.001 0.672 0.483

0.012 0.059 0.164

0.680 0.050 0.910

<0.001 0.752 0.049

0.029 <0.001 0.010

0.162 0.011 0.977

0.126 0.185 0.810

P-value D effect S effect D × S interaction x–z

0.011 0.094 0.827

Means in the same column without common superscripts differ significantly at P≤0.05. SD for all birds divided by the square root of the number of turkeys.

a

3. Results Sodium levels in the diet affected (P<0.05; 0.8 vs. 1.3 and 1.8 g/kg) the final BW of turkeys at the age of 18 wk (Table 3). In each subsequent 4 wk feeding period, until 12 wk of age, the growth rate of birds was affected by sodium levels. All levels higher than 0.8 g/kg increased BWG in turkeys. At a later stage (wk 13–18), there were no differences (P>0.05) in BWG between treatments due to sodium levels in the diet (P=0.680). Sodium sources had no effect (P>0.05) on the final BW of turkeys. However, in the starter period (0–4 wk), BWG was affected (P<0.05) by sodium sources; NaCl treatment showed higher BWG compared with NaHCO3 and Na2 SO4 salts (P<0.001); an opposite trend was observed in the final 13–18 wk of feeding (P<0.05; NaCl vs. NaHCO3 and Na2 SO4 ). During wk 0–4 and 5–8, a sodium level by source interaction for FCR was noted (P=0.049 and P=0.010, respectively). In wk 0–4, FCR values for the 0.8 g/kg and 1.8 g/kg Na dosage were similar in all three salt types; whereas at the medium dietary Na level (1.3 g/kg), an increase in FCR was found in turkeys fed a diet with NaHCO3 , compared with those receiving an NaCl-supplemented diet (P<0.05). During wk 5–8, the FCR in the 1.3 and 1.8 g/kg supplemented groups were unaffected, while in the lowest Na group, NaCl supplementation increased FCR in turkeys. In wk 9–12, FCR was affected by sodium sources (P=0.011; NaCl vs. NaHCO3 and Na2 SO4 ). No differences in FCR were observed in the last feeding period (wk 13–18). The mortality rates were considered normal for the growth rate of turkeys (overall mean of 5.88%), and they were not affected (P>0.05) by the treatments. The moisture content of excreta on d 49 was not affected (P>0.05) by sodium levels or sources, however, on d 112 the moisture content of excreta was affected (P<0.05) by sodium levels. Supplementation of 0.8 g Na/kg increased the moisture content of excreta in comparison with the 1.8 g/kg treatment (Table 4). Sodium levels and sources had no effect (P>0.05) on the FPD score. Increasing sodium levels in the diet increased (P<0.05; 0.8 vs. 1.8 g/kg) serum Mg, P, Na, and Cl concentrations in turkeys after 18 wk experimental feeding (Table 5). A sodium level by source interaction (P<0.001) on serum K concentrations was observed. In turkeys fed low-sodium diets, serum K concentrations decreased compared with the NaCl treatment, while in birds fed high-sodium diets serum K concentrations did not differ subject to salt types. Sodium levels had no effect (P>0.05) on the relative full weight of the small intestine, the viscosity and DM concentrations of the jejunal and ileal digesta (Table 6), however, some effects of sodium sources were noted. Viscosity and DM concentrations in the jejunum and ileum were increased by NaHCO3 in comparison with the NaCl treatment. While the jejunal pH was not affected by dietary treatments, a sodium level by source interaction was observed (P<0.05) for ileal pH. At the low sodium level, NaHCO3 reduced ileal pH in comparison with the other sodium sources, whereas at the high Na level ileal pH varied in response to different Na salts. Caecal environment indices were not affected by Na levels in the diet except for ammonia concentrations which were found to decrease (P<0.05) at the low Na level in comparison with the high Na level, but several changes due to the sodium source were observed (Table 7). The relative weight of caecal digesta decreased in response to NaHCO3 compared with NaCl and Na2 SO4 , the moisture content of caecal digesta decreased in the NaCl treatment, compared with Na2 SO4 , and the activity levels of ␤-glucosidase and ␤-glucuronidase in the caecal contents increased in response to NaHCO3 compared with NaCl and Na2 SO4 .

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Table 4 Dry matter (DM) content of excreta and foot pad dermatitis (FPD) score in turkeys fed diets with different Na salts. Additional Na/source

DM of excreta (g/kg)

NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 SEMa Dosage effect (D)

Day 49

Day 112

Day 55

Day 125

1.8 g/kg 1.3 g/kg 0.8 g/kg

199.7 196.9 201.4 203.6 202.1 201.4 201.1 201.0 210.5 1.35 199.3 202.4 204.2

201.2 217.9 214.5 202.2 221.9 213.0 227.4 221.0 218.9 2.21 211.2y 212.4xy 222.4x

1.9 1.7 1.7 1.7 1.7 1.6 1.7 1.6 1.4 0.05 1.8 1.7 1.5

2.8 2.9 2.8 2.7 2.7 2.9 2.5 2.7 2.5 0.07 2.8 2.7 2.6

NaCl NaHCO3 Na2 SO4

201.5 200.0 204.4

210.3 220.3 215.5

1.8 1.7 1.5

2.7 2.8 2.7

0.223 0.187 0.831

0.323 0.872 0.857

1.8 g/kg

1.3 g/kg

0.8 g/kg

Salt effect (S)

P-value D effect S effect D × S interaction x–y

FPD score

0.336 0.393 0.640

0.050 0.158 0.206

Means in the same column without common superscripts differ significantly at P≤0.05. SD for all birds divided by the square root of the number of turkeys.

a

The higher sodium level increased (P<0.05) the content of acetic, propionic, iso-butyric and valeric acids as well as total SCFA concentrations in the caecal digesta (Table 8). An effect of sodium source (P<0.05) on iso-butyrate concentrations was observed, NaHCO3 increased caecal iso-butyrate concentrations compared with NaCl and Na2 SO4 . A sodium level by source interaction was observed for acetic and valeric acids, and total SCFA concentrations. Acetate and total SCFA concentrations increased in response to NaHCO3 at the low Na level, and decreased at the high Na level, in comparison with the other types of Na salts. Valeric acid concentrations increased in response to Na2 SO4 at the high Na level but not at the low Na level, when compared with the other types of Na salts. Neither sodium level nor source affected (P>0.05) carcass dressing percentage, thigh yield and shank yield (Table 9), while breast muscle yield decreased (P<0.05) in response to sodium source (NaHCO3 vs. Na2 SO4 ). A D × S interaction (P=0.046) revealed that NaHCO3 applied at a lower dose reduced pH15min in the breast muscle, compared with the 1.8 g/kg dose. Interestingly, an Na level by source interaction occurred, indicating that NaHCO3 and Na2 SO4 salts used as NaCl alternatives caused an increase (P=0.049) in the L* value (lightness) of the breast muscle (Table 10). No differences (P>0.05) in the other meat colour parameters (a*, b*) due to the sodium level or source were detected.

Table 5 Serum biochemical parameters in turkeys fed diets with different Na salts. Additional Na/source NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 SEMa

Mg (mmol/L) 1.00 1.8 g/kg 0.99 0.98 0.85 0.8 g/kg 0.96 0.93 0.030

P (mmol/L) 1.81 1.87 1.87 1.55 1.65 1.58 0.109

Ca (mmol/L) 2.50 2.52 2.42 2.35 2.42 2.40 0.087

Na (mmol/L) 154 154 153 148 151 149 0.7

Cl (mmol/L) 117 116 117 114 114 114 0.5

K (mmol/L) Urea (mmol/L) 3.11xy 0.36 2.81y 0.36 3.63xy 0.36 3.94x 0.41 3.13xy 0.41 2.70y 0.36 0.097 0.033

Uric acid (␮mol/L) 202 209 239 186 210 199 0.2

Creatinine (␮mol/L) 10.7 14.5 14.5 13.0 15.2 10.7 0.21

Dosage effect (D)

1.8 g/kg 0.8 g/kg

0.99x 0.91y

1.84x 1.58y

2.47 2.40

154x 149y

117x 114y

3.19 3.26

0.36 0.39

217 199

13.0 13.0

Salt effect (S)

NaCl NaHCO3 Na2 SO4

0.93 0.98 0.95

1.68 1.76 1.72

2.42 2.47 2.41

152 152 151

115 115 115

3.52x 2.97y 3.16xy

0.38 0.38 0.36

194 209 219

11.8 14.8 12.6

<0.001 0.158 0.054

<0.001 0.530 0.905

P-value D effect S effect D × S interaction x–y

0.058 0.494 0.597

0.001 0.433 0.364

Means in the same column without common superscripts differ significantly at P≤0.05. SD for all birds divided by the square root of the number of turkeys.

a

0.023 0.879 0.741

0.631 0.013 <0.001

0.166 0.611 0.611

0.448 0.675 0.771

0.999 0.197 0.197

80

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Table 6 Effect of dietary Na source and level on the small intestinal parameters. Full weight (g/kg BW)b

Additional Na/source

Jejunum Ph

NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 SEMa Dosage effect (D) Salt effect (S)

Ileum Viscosity (mPas)

c

DM (g/kg)

pH x

Viscosity (mPas)

DMc (g/kg)

0.8 g/kg

15.29 16.61 15.68 14.94 16.78 16.01 0.321

5.99 6.07 5.95 6.01 5.73 5.94 0.039

1.810 2.004 1.917 1.656 2.146 1.921 0.043

168.0 199.6 189.0 157.9 188.9 170.9 4.460

6.65 6.51x 6.52x 6.63x 5.52y 6.70x 0.110

1.641 2.093 2.091 1.581 2.189 2.204 0.082

15.62 178.6 171.5 154.2 186.4 146.5 3.970

1.8 g/kg 0.8 g/kg NaCl NaHCO3 Na2 SO4

15.68 15.91 15.11 16.69 15.84

6.00 5.89 6.00 5.90 5.94

1.910 1.907 1.733y 2.075x 1.919xy

185.5 175.9 162.9y 199.2x 179.9xy

6.56 6.29 6.64x 6.02y 6.61x

1.941 1.991 1.611y 2.141x 2.148x

168.7 162.4 155.2y 182.5x 159.0y

0.150 0.563 0.105

0.971 0.003 0.302

0.156 0.018 0.041

0.749 0.009 0.880

1.8 g/kg

P-value D effec S effect D × S interaction

0.938 0.152 0.904

0.230 0.003 0.672

0.369 0.006 0.161

x–y

Means in the same column without common superscripts differ significantly at P≤0.05. SD for all birds divided by the square root of the number of turkeys. b Body weight. c Dry matter. a

4. Discussion An analysis of diets fed to turkeys revealed that Na and Cl content was close to the anticipated values. Potassium was supplied exclusively by feed raw ingredients, and the diets for subsequent feeding periods contained decreasing levels of K, due to a decreasing content of soy bean meal. The DEB for each diet is expressed as analysed Na + K − Cl, mEq/kg. Some DEB values for the starter period (0–4 wk) exceeded 250 mEq/kg, often recommended as the maximum value for young turkeys (Frame et al., 2001), in particular when the alternatives to dietary NaCl were used as additional Na sources (NaHCO3 and Na2 SO4 ). Earlier studies have reported a decrease in the live weight of young turkey poults at DEB 250 mEq/kg or higher (Frame et al., 2001). There has been a growing interest among poultry nutritionists in Na sources alternative to NaCl, due to the reported synergistic effect of high dietary Na and Cl levels on increased water consumption, followed by elevated hydration of the intestinal contents and increased litter moisture (Mushtaq et al., 2005). As compared with NaCl, which is inexpensive and commonly used in poultry nutrition, NaHCO3 has been claimed to be a good source of Na for birds since it has a beneficial Table 7 Effect of dietary Na source and level on the caecal environment indices. Additional Na/source

Tissue (g/kg BWb ) 3.29 3.32 3.27 3.19 3.34 3.56 0.057

Digesta (g/kg BWb ) 1.68x 0.83z 1.31y 1.24y 0.90z 1.44xy 0.064

DMc (g/kg)

pH

156.1 171.4 202.9 172.5 194.5 198.3 4.77

Ammonia (mg/g) 0.42 0.42 0.41 0.33 0.37 0.34 0.015

6.13 6.57 6.00 6.43 6.53 6.39 0.084

␤-glucosidase (␮mol/h/g digesta) 6.83 10.40 9.45 6.09 10.53 8.36 0.517

␤-glucuronidase (␮mol/h/g digesta) 15.47 22.82 14.66 12.23 24.35 18.98 1.242

NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 SEMa

1.8 g/kg

Dosage effect (D)

1.8 g/kg 0.8 g/kg

3.25 3.36

1.27 1.19

176.9 188.4

0.42x 0.34y

6.23 6.45

8.89 8.33

17.65 18.53

Salt effect (S)

NaCl NaHCO3 Na2 SO4

3.24 3.33 3.41

1.46x 0.86y 1.38x

164.3y 182.9xy 200.6x

0.37 0.39 0.37

6.28 6.55 6.20

6.46y 10.47x 8.90x

13.85y 23.60x 16.82y

0.020 0.803 0.854

0.196 0.207 0.557

0.554 0.005 0.864

0.693 0.003 0.377

P-value D effect S effect D × S interaction x–z

0.8 g/kg

0.574 0.483 0.374

0.415 <0.001 0.037

0.178 0.005 0.390

Means in the same column without common superscripts differ significantly at P≤0.05. SD for all birds divided by the square root of the number of turkeys. b Body weight. c Dry matter. a

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Table 8 Effect of dietary Na source and level on the caecal environment indices. Additional Na/source

Short-chain fatty acid (SCFA) (␮mol/g of caecal digesta) Acetic

Propionic

Iso-butyric

Butyric

Iso-valeric

Valeric

Total SCFA

0.8 g/kg

66.11x 55.07xy 65.67x 48.74y 60.44xy 50.73y 2.051

25.51 21.06 27.09 17.06 21.45 20.15 1.092

0.48 1.04 0.65 0.72 0.99 0.78 0.051

17.25 16.32 15.61 12.01 16.77 12.87 0.630

0.54 0.92 0.74 0.56 0.80 0.79 0.053

2.58y 2.57y 3.88x 1.95y 2.70y 2.04y 0.146

116.07x 101.50xy 118.91x 84.27y 107.63xy 90.97y 3.544

Dosage effect (D)

1.8 g/kg 0.8 g/kg

62.28x 53.30y

24.55x 19.55y

0.72 0.83

16.39x 13.89y

0.74 0.72

3.01x 2.23y

112.16x 94.29y

Salt effect (S)

NaCl NaHCO3 Na2 SO4

57.43 57.75 58.20

21.29 21.25 23.62

0.60y 1.01x 0.71y

14.63 16.54 14.24

0.55 0.86 0.77

2.27 2.63 2.96

100.17 104.56 104.94

0.861 0.054 0.789

0.002 0.059 0.005

NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 SEMa

1.8 g/kg

P-value D effect S effect D × S interaction x–z

0.022 0.986 0.035

0.020 0.561 0.183

0.232 0.001 0.401

0.039 0.241 0.152

0.008 0.791 0.036

Means in the same column without common superscripts differ significantly at P≤0.05. SD for all birds divided by the square root of the number of turkeys.

a

influence on blood pH and H+ ion balance. Moreover, some authors have reported that dietary NaHCO3 excelled NaCl as a Na source under thermal stress conditions (Ahmad and Sarwar, 2006; Mushtaq et al., 2007). In the present study, a decrease in dietary Na addition from 1.8 to 0.8 g/kg significantly reduced excreta moisture on day 112 of the study, but the type of the applied salt had no influence on the above parameter. The applied dietary treatments did not affect the FPD score, presumably due to the fact that the highest Na dosage did not substantially exceed turkey requirements for this microelement, thus proving that the calculated DEB is of lesser importance unless enormous amounts of Na, K or Cl are added to a diet. In a recent work of Jankowski et al. (2011b) reporting two experiments on broiler chickens fed diets with different Na addition (up to 2.5 g/kg), the use of NaHCO3 and Na2 SO4 , in particular the latter, significantly reduced excreta moisture and diminished the FPD score. The results of the present study point to worse FCR and a slower growth rate in turkeys fed a diet with the lowest Na addition (0.8 g/kg) over the first 8 and 12 wk of feeding, respectively. Considering the aim of this study, the feeding system with 1.3 or 1.8 g/kg additional Na resulted in comparable final BW of turkeys, while a reduction in dietary Na to 0.8 g/kg led to significantly worse turkey performance. Our findings also indicate that when contributing equal amounts of Na, a more desirable FCR may be achieved in turkeys upon dietary NaHCO3 and Na2 SO4 than NaCl. Firman (2010) has recently proposed the formulation of ideal protein-based diets for turkeys, including a mixture of NaCl and NaHCO3 at a proportion of 60:40. Table 9 Effect of dietary treatments on the carcass characteristics of turkeys. Additional Na/source

Dressing, g/kg

Component yields (g/kg of body weight)

pH of breast muscle

Breast

Thigh

Shank

Abdominal fat

pH15

0.8 g/kg

828.0 826.8 831.2 829.5 808.4 816.6 2.88

244.0 232.6 237.2 246.8 228.1 234.3 2.44

108.9 112.9 110.9 110.7 109.6 113.1 1.13

75.6 76.2 78.6 79.4 76.3 79.6 0.82

7.60 8.30 8.90 7.80 7.50 6.30 0.390

6.10xy 6.20y 6.03xy 6.09xy 6.00x 6.13xy 0.025

5.89 6.01 5.91 5.77 5.81 5.94 0.030

5.70 5.71 5.66 5.69 5.61 5.71 0.016

Dosage effect (D)

1.8 g/kg 0.8 g/kg

828.7 818.8

237.9 236.4

110.9 111.1

76.8 78.5

8.60 7.20

6.11 6.07

5.94 5.84

5.69 5.67

Salt effect (S)

NaCl NaHCO3 Na2 SO4

828.7 817.6 823.9

245.4x 230.4y 235.7xy

109.8 111.2 112.0

77.5 76.2 79.1

8.20 7.90 7.60

6.09 6.10 6.08

5.83 5.91 5.92

5.70 5.66 5.68

0.081 0.836 0.592

0.424 0.935 0.046

0.104 0.352 0.290

0.549 0.674 0.171

NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 SEMa

P-value D effect S effect D × S interaction x–y

1.8 g/kg

0.063 0.267 0.303

0.744 0.042 0.807

0.923 0.743 0.581

Means in the same column without common superscripts differ significantly at P≤0.05. SD for all birds divided by the square root of the number of turkeys.

a

0.326 0.370 0.646

min

pH1

h

pH24

h

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Table 10 Effect of dietary Na source and level on breast muscle quality. Meat colour parametersb

Additional Na/source

NaCl NaHCO3 Na2 SO4 NaCl NaHCO3 Na2 SO4 SEMa Dosage effect (D) Salt effect (S)

P-value D effect S effect D × S interaction

Cooking loss (g/kg)

L*

a*

b*

1.8 g/kg 0.8 g/kg

53.18 54.50 54.57 52.57 54.80 54.98 0.347 54.08 54.11

4.58 4.24 4.83 5.74 4.60 4.45 0.179 4.55 4.93

10.47 9.79 11.75 10.92 11.37 10.77 0.237 10.67 11.02

146.3 129.2 163.1 140.5 181.0 132.5 7.08 146.2 151.3

NaCl NaHCO3 Na2 SO4

52.87y 54.65x 54.77x

5.16 4.42 4.64

10.69 10.58 11.26

143.4 155.1 147.8

1.8 g/kg

0.8 g/kg

0.961 0.049 0.801

0.283 0.220 0.213

0.455 0.442 0.089

0.716 0.785 0.057

x–y

Means in the same column without common superscripts differ significantly at P≤0.05. SD for all birds divided by the square root of the number of turkeys. b L*, lightness; a*, redness; b*, yellowness. a

Only very few experiments have dealt with a comparison of different Na salts in turkey nutrition. One study has shown that turkeys raised at a relatively high environmental temperature and humidity gain better if their diets are supplemented with NaHCO3 (Bonsembiante et al., 1990). Our previous work involving broilers (raised at a standard environmental temperature) has demonstrated that in comparison with NaHCO3 , Na2 SO4 is a better alternative to NaCl in terms of feed utilisation during the starter period (Jankowski et al., 2011b). According to some authors, birds may relatively well tolerate a high dietary Na content, but insufficient Na levels may cause blood electrolyte disturbances (Mushtaq et al., 2007; Olanrewaju et al., 2007), leading to a slower growth rate of birds and worse feed utilisation, as noted in the present experiment. Surprisingly, the type of the applied Na salt did not affect serum biochemical parameters in turkeys. In an earlier study of broiler chickens, the applied dietary treatments ranging from 2.3 to 7.3 g/kg Na, from 2.6 to 9.9 g/kg Cl, at DEB of 327–700 mEq/kg, did not influence the serum concentrations of Ca, Na, K, Cl, P, and Mg (Johnson and Karunajeewa, 1985). Our recent work on broilers also confirmed that a considerable deficiency in dietary Na levels significantly affects the blood electrolyte profile (Tykalowski et al., 2011). Numerous authors have observed higher water consumption in birds fed diets containing an increased amount of Na, which may result in increased hydration of the small and large intestinal digesta (Mushtaq et al., 2007; Jankowski et al., 2011a). Surprisingly, in the present experiment the dietary Na levels did not affect small intestinal viscosity and dry matter concentration of the jejunal, ileal and caecal contents, while the type of Na salt did. The lowest DM concentration of digesta in the analysed gastrointestinal segments was noted in the NaCl treatment, and both alternative salts beneficially increased digesta DM. However, some differences between dietary NaHCO3 and Na2 SO4 were observed – the former affected small intestinal DM concentration, and the latter caecal DM concentration. The present results indicate that NaHCO3 and Na2 SO4 can be recommended as dietary tools supporting the maintenance of proper hydration of the intestinal digesta and prevention of health related to increased litter moisture problems in poultry. A previous study on broilers has shown that carbohydrate fermentation, as indicated by caecal SCFA production rates, were increased under a moderate dietary increase in NaCl content (Jankowski et al., 2011a). In the present experiment, the above trend was noted in the NaCl and Na2 SO4 treatments, but not when NaHCO3 was added to a diet, and it was further validated by total caecal SCFA concentrations determined in experimental groups. The caecal pH value, however, was not affected by dietary treatments in the present experiment. Previous work on broilers (Jankowski et al., 2011b) has shown no differences between different dietary Na salts (the same as in the present study) with respect to carcass dressing percentage and breast muscle yield. In the current experiment, sodium levels had no effect on the yields of individual carcass components which, however, were affected by sodium sources as indicated by a decrease in breast muscle yield in response to NaHCO3 , compared with the NaCl treatment. Further investigation is required here since some experiments involving broilers (Hooge et al., 1999) have pointed to a lower breast muscle yield in birds fed diets containing Na2 SO4 , compared with those fed diets supplemented with NaCl or NaHCO3 . Abdominal fat content was similar among groups in the present experiment, indicating a comparable energy use rate in all birds. A substantial increase in abdominal fat content should be considered as an undesirable attribute of meat quality (Mushtaq et al., 2005; Kowalska et al., 2011). As demonstrated by Webb and Casey (2010), turkeys selected for fast growth may be in danger of pale, soft, and exudative (PSE)-like meat occurrence. Some authors have suggested the use of colour score measurements, particularly L* values, in the assessment of the risk factors for meat becoming PSE (McCurdy et al., 1996), while others have shown that lightness (L*) is well correlated with meat pH and water-holding capacity (Owens and Sams, 2000). It has been reported that an undesired, rapid drop in meat pH values results from increased post-mortem glycolysis

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while muscle temperature remains relatively high; this may lead to increased protein denaturation and subsequently to a lighter meat colour, increased weight loss while cooking, and softer texture (Owens et al., 2009). Based on the 15 min post-mortem breast meat pH, Rathgeber et al. (1999) classified turkey meat as rapidly glycolysing at pH lower than 5.80, and as normal when pH values were higher than 6.00. In the present study, all dietary treatments were characterised by similar cooking loss and by breast muscle pH15 min values above 6.00, in the latter case except for the dietary treatment with 0.8 g/kg additional Na originating from NaHCO3 (pH15 min = 6.00). Based on the values obtained in the study, the analysed breast muscles should be considered normal turkey meat. However, due to increased breast meat lightness in the NaHCO3 and Na2 SO4 treatments, the consumer acceptance of the product could vary subject to the Na salt used. This issue should be monitored thoroughly. 5. Conclusion It can be concluded that a low Na dose (0.8 g/kg) has an adverse influence on the growth performance of turkeys and feed utilisation, in particular at the early stages of feeding, compared with birds treated with 1.3 or 1.8 g/kg additional Na. Although both alternative Na salts, NaHCO3 and Na2 SO4 , improved feed utilisation, their use as feed ingredients should be closely monitored as some disadvantages, i.e. a decreased breast muscle yield upon dietary NaHCO3 treatment and increased lightness of breast meat upon diet supplementation with both alternative salts, were found in the present study. Acknowledgements This work was supported by the National Centre for Research and Development, grant no. N R 12 0096 06. References Ahmad, T., Sarwar, M., 2006. Dietary electrolyte balance: implications in heat stressed broilers. World Poult. Sci. J. 62, 638–653. Bonsembiante, M., Chiericato, G.M., Bailoni, L., 1990. Use of sodium bicarbonate in diets for meat turkeys reared at a high environmental temperature and humidity. Rev. Avic. 59, 37–41. Borges, S.A., Fischer da Silva, A.V., Ariki, J., Hooge, D.M., Cummings, K.R., 2003. Dietary electrolyte balance for broiler chickens exposed to termoneutral or heat–stress environments. Poult. Sci. 82, 428–435. Firman, J.D., 2010. Ideal protein based diets for turkeys. Int. J. Poult. Sci. 9, 856–862. Frame, D.D., Hooge, D.M., Cutler, R., 2001. Interactive effects of dietary sodium and chloride on the incidence of spontaneous cardiomypoathy (round heart) in turkeys. Poult. Sci. 80, 1572–1577. Francesch, M., Brufau, J., 2004. Nutritional factors affecting excreta/litter moisture quality. World Poult. Sci. J. 60, 64–75. GfE (Society of Nutrition Physiology), 1999. Empfehlungen zur Energie - und Nährstoffversorgung der Legehennen und Masthühner (Broiler). DLG Verlag, Frankfurt am Main. Hocking, P.M., Mayne, R.K., Else, R.W., French, N.A., Gatclffe, J., 2008. 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Effect and interactions of dietary sodium and chloride on broiler starter performance (hatching to twenty-eight days of age) under subtropical summer conditions. Poult. Sci. 84, 1716–1722. Mushtaq, T., Aslam, M.M., Athar, M., Hooge, D.M., Ahmad, T., Ahmad, G., Mushtaq, M.M.H., Noreen, U., 2007. Dietary sodium and chloride for twenty-nine to forty-two-day-old broiler chickens at constant electrolyte balance under subtropical summer conditions. J. Appl. Poult. Res. 16, 161–170. NRC, 1994. Nutrient Requirements of Poultry, National Research Council, 9th edition. National Academy Press, Washington, DC. OJEU, 2010. Directive 2010/63/EU of the European Parliament and of the Council on the protection of animals used for scientific purposes. Official Journal of the European Union, 33–79, OJEU 20. 10. 2010, Series L 276. Olanrewaju, H.A., Thaxton, J.P., Dozier, W.A., Branton, S.L., 2007. Electrolyte diets, stress, and acid-base balance in broiler chickens. Poult. Sci. 86, 1363–1371. Owens, C.M., Alvarado, C.Z., Sams, A.R., 2009. Research developments in pale, soft, and exudative turkey meat in North America. Poult. Sci. 88, 1513–1517. Owens, C.M., Sams, A.R., 2000. The influence of transportation on turkey meat quality. Poult. Sci. 79, 1204–1207. Rathgeber, B.M., Boles, J.A., Shand, P.J., 1999. Rapid postmortem pH decline and delayed chilling reduce quality of turkey breast meat. Poult. Sci. 78, 477–484. ´ Z., Ju´skiewicz, J., Koncicki, A., 2011. Level of electrolytes and percentage of T-lymphocyte Tykalowski, B., Stenzel, T., Mikulski, D., Jankowski, J., Zdunczyk, subpopulations in blond of broiler chickens fed mixtures with a different content of sodium chloride. Bull. Vet. Inst. Pulawy 55, 333–337. Watkins, S.E., Fritts, C.A., Yan, F., Wilson, M.L., Waldroup, P.W., 2005. The interaction of sodium chloride levels in poultry drinking water and the diet of broiler chickens. J. Appl. Poult. Res. 14, 55–59. Webb, E.C., Casey, N.H., 2010. 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