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Eight-weeks-old male turkeys (n=60) were randomly distributed in light-proof rooms containing 12 floor pens (5 birds per fresh wood shavings litter pen). In a completely randomized design experiment, birds were divided and fed by different levels of terbutaline (TE0=0, TE1=7.5 and TE2=15 mg /kg/day/dry matter). After 16 weeks, carcass weight, carcass efficiency, skeletal muscle composition and blood parameters were determined. Dietary trebutaline significantly increased the carcass weight, carcass efficiency (P < 0.05) and breast and thigh muscle weight (P < 0.01). On the other hand, 7.5 mg kg-1 terbutaline significantly (P < 0.05) decreased abdominal fat. The blood glucose, T4, T3 (P < 0.01) triglyceride and cholesterol (P < 0.05) were increased and insulin (P < 0.01), urea and uric acid (P < 0.05) were decreased by terbutaline. Dietary treatments had no effect on the concentration of aspartate aminotransferase, alanine aminotransferase creatine kinase, alanine and glutamine. Results showed that 7.5 mg kg-1 terbutaline in the turkey diet increased body weight gain and carcass efficiency. In addition, it can improve the feed conversion ratio.
Key words: Beta-adrenergic, performance, carcass trait, blood parameter, turkey
Short title: Terbutaline and blood parameter
There are nine different types of adrenergic receptors: α1A, α1B, α1D, α2A, α2B, α2C, β1, β2 and β3. However, adipocytes express a combination of five different adrenoreceptor isoforms: α1, α2, β1, β2 and β3. It is necessary to mention that lipolysis is signaled by Beta-adrenergic (βAR). The β2 receptors (the most common type of β receptors) are present in liver, skeletal muscle and other tissues and are involved in the mobilization of fuels (such as the release of glucose through glycogenolysis) (Metzler 2004; Smith and Marks 2004; Vance and Vance 2008). The former show an almost equal affinity for epinephrine and nor-epinephrine (catecholamines). The latter are considered to be more sensitive to epinephrine than nor-epinephrine (Barisione and Baroffio 2010). In general, the effects of βAR agonists are improved feed utilization efficiency, increased leanness, increased dressing percentage (carcass weight/live weight), increased rate of weight gain, decreasing carcass fat, and increasing protein deposition and carcass yield. Beginning in the early 1980s, these effects have been demonstrated in several species including lambs, broilers, turkeys, beef cattle and swine by using several synthetic βAR agonists such as cimaterol, ractopamine, salbutamol, clenbuterol, metaproterenol and isoproterenol (Dalrymple et al. 1984; Scholtyssek 1988; National Research Council 1990; Buyse and Decuypere 1991; Ji and Orcutt 1991; Smith 1998; Hamano and Sugawara 1999; Fawcett et al. 2004; Mersmann 2002; Anderson and Moody 2004; Tahmasbi et al. 2006). In addition to a variable response observed in different species, even when the same βAR agonist is administered in a specific species, there is considerable variation because several factors including diet, dosage and duration of treatment, age, weight and genetics have been shown to influence the response to β-agonists and are important to the successful use of β-agonists in livestock (Mersmann 2002; Anderson and Moody 2004). The βAR agonists specifically enhance the growth of muscle and give a small reduction in the growth of fat. Their effects are mediated by modifying specific metabolic signals in muscle and fat cells with a resulting increase in nutrients directed towards lean growth (Anderson and Moody 2004) so that the results of feeding repartitioning agents include consistently reduced fat accretion accompanied by an increase in muscle mass. Any proposed mechanism must begin with the possibility of the direct effects of the agonists on skeletal muscle and adipocyte βAR receptors. βAR agonists cause modification of metabolite concentrations and adipocytes (Mersmann 1998; Beermann 2002; Mersmann 2002; Nourozi et al. 2008). Of course, many aspects of these pharmacodynamic properties of the agonist are coupled with the blood flow to the target organs (Mersmann 2002) although the anabolic response of muscle in endocrine-altered animals to βAR agonist administration adds support to mechanism(s) independent of hormone modulation (Bates and Pell 1991). The β-receptor is directly coupled to the guanine nucleotide-dependent phospholipase C. Thus, the βAR receptor can couple independently to both adenylyl cyclase and to phospholipase C. Most of the βAR receptor sites have been mapped in the spinal cord and cerebellum of the domestic fowl using a fluorescent βAR antagonist 9-amino-acridin-propanolol (Stevens 1996). The stimulation of skeletal muscle growth by βAR agonists may involve modulation of normal endocrine influences on growth and metabolism (Beermann 2002). Despite these positive effects, interest in the use of β-agonists in meat producing animals declined in the early nineties following outbreaks of severe allergic reactions attributed to the consumption of livers from cattle treated with clenbuterol, and the European Union subsequently banned their use (Mazzanti et al. 2003; Fawcett et al. 2004). So far, to our knowledge no studies have reported the effects of oral administration of terbutaline on carcass traits and blood parameters of turkey. This study endeavours to evaluate the effects of terbutaline on carcass composition and blood parameters in tom turkey.
Materials and methods
Sixty male turkeys (8 weeks old) were randomly distributed to 3 treatments in 12 groups of 5 birds, with 4 replicates per treatment. The treatments were T0 (Control): 0 mg terbutaline /kg/day/dry matter, T1: 7.5 mg terbutaline /kg/day/dry matter, and T2: 15mg terbutaline /kg/day/dry matter administered with feed. The diets were formulated to meet or exceed National Research Council requirements (NRC 1994). The composition and nutrient content of basal diets are shown in table 1. Feed and water were provided ad libitum. The tom turkeys were kept in 12 light-proof rooms (5 birds per fresh wood shavings litter pen) in Tatar Animal Science Research Center, East Azarbaijan, Iran. The experimentation procedure was based on Bio security Rules of Iran Agricultural Ministry. The experiment lasted 8 weeks. The daily photoperiod during the experiment was 23L:1D. Data on performance (average daily feed intake, live body weight and feed conversion ratio) were recorded. At the end of the experiment (16-week age), all birds were weighed and killed by severing the jugular vein, bled for almost 3-4 min, and defeathered. Carcasses were manually eviscerated, washed, and allowed to drip. The liver and heart were expressed as percentages of body weight, and abdominal fat, which consisted of fat surrounding the gizzard, proventriculus and that in the abdominal body cavity, was removed and weighed immediately to the nearest milligram. Carcass and carcass parts yield (including thighs and breasts) data were also collected. Blood samples (5ml) were randomly collected from three birds from each replicate pen by venipuncture of the vena ulnaris without anticoagulant to obtain serum by Terumo syringe with a needle (0.7-32 mm) at the end of the experiment. Sera were harvested by centrifugation at 3000 - g for 10 min at room temperature and were frozen for blood parameters' assay. Blood total triiodothyronine (T3), thyroxine (T4), thyroid stimulating hormone (TSH) and insulin concentrations were determined via radioimmunoassay using commercially available reagent kits (Kavoshyare Noor Co., Tehran, Iran) according to the procedure of Kloss et al. (1994). Blood glucose, cholesterol, triglycerides, urea and uric acid concentrations were measured by enzymatic-calorimetric methods, blood creatine kinase (CK), aspartate aminotransferase (AST) and alanine aminotransferase (ALT) were measured by IFCC (International Federation of Clinical Chemistry Scientific Committee) method, and blood glutamine and alanine concentrations were determined by HPLC. Data were analyzed by the ANOVA procedure of SAS software (SAS Institute 1986, SAS Institute Inc., Cary, NC, USA). All percentage data were subjected to arc sine transformation (Steel and Torrie 1960). A mean comparison was accomplished using Duncan's multiple-range test (Duncan 1955), and a probability value of less than 0.01 and 0.05 was considered statistically significant unless otherwise noted.
The results of mean body weight (bwt), feed intake and feed conversion ratio (FCR) for all treatments along with a mean comparison are summarized in table 2. Birds receiving a terbutaline-supplemented diet gained significantly greater weight and consumed more feed compared to controls throughout the experiment (weeks 8-16) (P < 0.01). Generally, terbutaline supplementation significantly (P < 0.01) decreased FCR throughout the experiment. The mortality rate in all groups was similar to standard one without any significant difference. Carcass weight, carcass performance, proportional weight of liver, abdominal fat pad, and heart, breast and thigh weight are summarized in table 2. The proportional weight of heart and liver was not affected by terbutaline supplementation. Terbutaline-supplemented groups had greater (P < 0.05) carcass weight and carcass efficiency and breast and thigh weight than the control group. Abdominal fat weight decreased (P < 0.05) by terbutaline supplementation, especially in the group receiving 7.5 mg kg-1 terbutaline in its diet. The influence of terbutaline supplementation on skeletal muscle composition is summarized in table 3. Terbutaline supplementation had no effect on the moisture content of the breast and thigh. On a fresh basis, the protein and fat contents of the breast and thigh were influenced (P < 0.01) by terbutaline supplementation. The protein content of the muscles increased while their fat content decreased in both terbutaline-supplemented groups compared to the control group. The effect of terbutaline supplementation on blood metabolites is presented in table 4. The blood glucose T4, T3 (P < 0.01), triglyceride and cholesterol (P < 0.05) levels were increased and blood insulin (P < 0.01), urea nitrogen and uric acid (P < 0.05) levels were decreased by terbutaline supplementation. Blood concentrations of CK, AST, ALT, alanine and glutamine were not affected by terbutaline supplementation.
In the present study birds were in excellent health throughout the experiment. Oral administration of any βAR agonist component usually causes an increase in daily weight gain which, in many cases, is accompanied by a slight decrease in feed intake, and as a consequence, efficiency of gain improves (Mersmann 2002). Of course, in the present study, feed intake increased significantly when compared to the experiment (table 2). It seems as if such a conflicting result is related to the variation among species as far as a response to a given βAR agonist is concerned (Mersmann 2002). An increase in breast and thigh weight in terbutaline groups in the present study is certainly due to the important role of βAR agonists in increasing blood flow to certain regions of the body. An increase in blood flow to the skeletal muscle may enhance the process of hypertrophy by the delivery of increased amounts of substrates and energy sources for protein synthesis. Likewise, increased blood flow to adipose tissue might carry nonesterified fatty acids away from the tissue to enhance the lipid degradation process. These mechanisms could readily augment the more direct effects of βAR agonists on the muscle cell and the adipocyte (Mersmann 1998). The relative weight of the liver and heart of birds fed terbutaline-supplemented diets was similar to those of controls (table 2). Our observation is similar to Fawcett et al. (2004), who fed broilers with R-salbutamol. The complexity of hormonal influences on skeletal muscle growth makes it necessary to separate possible indirect, endocrine-mediated actions of βAR agonists from direct, βAR-dependent mechanisms of action. Indirect modes of action of βAR agonists include possible perturbations in circulating concentrations, sensitivity, and(or) responsiveness to hormones known to influence skeletal muscle growth (Beermann 2002). In the present study, birds fed terbutaline-supplemented diets had a tendency towards a lower abdominal fat pad, which is in agreement with reports of Jones et al. (1985) and Takahashi et al. (1998). In animal production, β-agonists have been determined to be potent growth promoters, which lead to increased skeletal muscle mass and protein accretion or decreased fat deposition. In general, the βAR responsiveness is considered to be dependent on βAR receptor density (Kim and Sainz 1992; Hamano and Sugawara 1999). The decrease in carcass fat may be indicative of inhibition of lipid synthesis (Duquett and Muir 1982), while the reduction in the relative weight of abdominal fat pad may suggest lipolytic activity (Wellenreiter 1991). In the present study a decreased insulin level is a reasonable event for enhanced lipolysis, since insulin is well-known for its inhibitory role in lipolysis (Hazelwood 1999). In most βAR agonist-treated animals, there is a numerical decrease in carcass fat even if the data do not always achieve statistical significance. When comparative slaughter techniques are employed to calculate deposition rates, the rate of muscle or protein deposition is increased, whereas the rate of fat deposition sometimes is not significantly reduced (Chwalibog and Jensen 1996). Galbraith and Minassie (1997) obtained significant reductions on average in plasma urea and free fatty acids on day 9, and increases in plasma glucose concentration on day 49 in whether sheep treated with cimaterol. Of course some researchers believe that the increased blood glucose level due to isoproterenol, when given intensively, is generally transient and small (Hamano and Sugawara 1999; Reeds and Mersmann 1991; Hamano 2002). The pronounced increase in plasma glucose must be attributable to stimulated glycogenolysis (Hamano and Sugawara 1999; Hamano 2002). The existence of the contradictory results that seem to come from the same experimental design is caused by many factors - animal age, location of fat, duration of βAR agonist supplementation, feed composition, feeder design, feeding pattern, temperature, humidity, air flow in a building (influencing temperature, humidity, dust, toxic gasses, etc.), waste disposal system, season, breed, line, source, cage design, animal density in cages or pens, and randomization or placement of cages or pens in a room or building may influence the results (Buyse and Decuypere 1991; Wellenreiter 1991; Mersmann 1998 and 2002). In a study by Kim and Lee (1987), significant increases in plasma concentrations of fatty acid and triglycerides with the feeding of 10 ppm cimaterol were observed. In the present study, T3 and T4 levels were significantly increased by terbutaline supplementation (table 4). Hassanzadeh and Buyse (2002) showed the significantly greater T4 level by using atenolol. This may be due to higher T4 output by thyroid glands or by a reduced T4 degradation rate to reverse-T3. On the other hand, the thyroid hormone regulates the contractile properties of the heart as well as the expression of the alpha and beta heavy chains of myosin. Physiological levels of thyroid hormones may be an important modulator of the normal maturation of the βAR system in the developing ventricular myocardium (Olkowski 2007). Actually, birds are uricotelic and they excrete 80 % of their excess blood urea nitrogen as uric acid, with the result that the determination of the blood urea and uric acid is an appropriate measure to ascertain the amount of body amino acid metabolism (Sturkie 1986). When amino acid synthesis increases in muscle tissues, the amount of deamination, blood uric acid and urea nitrogen will decrease. This fact was observed in the present study so that by augmenting both levels of terbutaline in the diet the protein content of the breast and thigh was significantly increased and blood urea was dramatically decreased. As mentioned above, insulin inhibits lipolysis development in adipose tissue and thereby reduces the concentration of plasma-free fatty acids. As a result it abates the long-chain acyl-CoA, an inhibitor of lipogenesis (Murray and Granner 2003). In the present study, terbutaline supplementation leads to a steady reduction in serum insulin. It therefore seems as if terbutaline can increase the lipolysis amount and this terminates the reduction of abdominal fat and consequently expands the amount of carcass protein. In avian circulation, lipids are derived from intestinal absorption of dietary lipids, or mobilization from fat deposits and plasma triglyceride concentration is sufficiently well correlated with body fat content and can be used as an indirect means of selecting lean or fat broilers (Ansari-pirsaraei et al. 2007). In this experiment, increased serum cholesterol and triglycerides levels were observed in the terbutaline supplemented bird. In a study on the human subjects, terbutaline administration increased glycerol plasma concentration about twofold over mean basal concentrations in both males and females in a concentration-dependent fashion (Lima et al. 2005). Significant increases both in serum cholesterol and triglycerides of broiler chicks were also reported by Ansari-pirsaraei et al. (2007). It can be such explained that βAR agonist increased lipid metabolism in adipocytes. Activation of βAR causes an increase in cAMP that activates protein kinase A, which, in turn, phosphorylates hormone-sensitive lipase. Fatty acid synthesis and the esterification of fatty acids into triacylglycerols, the primary energy storage molecule in the adipocytes, are both inhibited by βAR agonists (Mersmann 2002; Horton et al. 2006). It also has been reported that β-agonist administration induced the lipolytic response and reduced lipoproteins' level (Buyse and Decuypere1991; Reeds and Mersmann 1991). Insulin stimulates glucose transport (Olefsky 1978) and lipogenesis (Haystead and Hardie 1986) in rat adipocytes. Catecholamines decrease insulin binding and inhibit insulin stimulation of glucose transport in isolated rat adipocytes (Kirsch et al. 1983). If these effects also occur in turkey adipose tissue, the observed insulin reduction in terbutaline groups could be explained by the same mechanisms. Byrem and Breemann (1998) showed that after 6 hours of infusion, simaterol directly induced a transient release of alanine from the cimaterol-infused hindlimb, which resulted in a slight decline in the net uptake of total amino acids. During βAR stimulation of skeletal muscle glycogenolysis and glycolysis, excess pyruvate is transaminated to form alanine, which is transported to splanchnic tissues for the production of glucose.
In summary, the result of the present study indicated a large effect of terbutaline on BWG and carcass composition. It significantly increased breast muscle weight by making use of β-agonists - an exciting prospect in modifying the composition of turkey meat towards a lower fat product. It can also be suggested that 7.5 mg /kg/day/dry matter terbutaline in the turkeys' diet is sufficient for increased body weight gain and carcass efficiency, but this important issue must be also take the fact into consideration that some studies demonstrated that β-agonists accumulated in some tissues such as liver (Malucelli and Ellendorfft 1994). A withdrawal period of more than 1 week is therefore sufficient to obtain acceptably low residue levels in all edible tissues.