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METABOLISM AND NUTRITION |
University of Guelph, Guelph, ON, Canada N1G 2W1
1 Corresponding author: sleeson{at}uoguelph.ca
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: polyamine • methionine • arginine • heat stress • broiler
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Under TN conditions, dietary Arg interacts with Met in birds through the creatine biosynthesis pathway. The growth-depressing effect of excessive levels of Met is partially alleviated when Arg, alone or in combination with glycine, is supplemented (Boorman and Fisher, 1966; Smith, 1968). Arginine transfers a guanidino group to glycine for the formation of glycocyamine, and the synthesis of creatine is completed by methylation of glycocyamine by S-adenosylmethionine (Bloch and Schoenheimer, 1941; Borsook and Dubnoff, 1945). Creatine can be stored in muscles or converted to creatinine, and both molecules could be excreted in the urine, resulting in clearance of methyl groups. However, under conditions of HS, such metabolism may be impaired, as suggested by the findings of Chamruspollert (2001), who reported decreased creatine and creatinine levels in excreta of birds under HS, without concomitant increase in the concentrations of these substances in muscle, which implies that birds under HS had lower creatine biosynthesis.
Other metabolic changes related to Arg metabolism are influenced by HS. The concentrations of ornithine, an amino acid synthesized from Arg by the enzyme arginase (Kawadaki et al., 1976), decreases under hyperthermic conditions (May et al., 1987; Balnave and Brake, 1999), possibly due to lower kidney arginase activity (Chamruspollert, 2001).
Putrescine (Put) is formed by the decarboxylation of ornithine, and spermine (Spm) and spermidine (Spd) can then be formed from Put in the presence of decarboxylated S-adenosylmethionine, which itself can be derived from Met. Thus, the formation of Spm and Spd in birds requires both Arg and Met. These biogenic amines are important for cell division, protein synthesis, and tissue growth (Seiler, 1992) and play a key role in gut function (Luk et al., 1980). The first step in polyamine biosynthesis is the formation of Put from ornithine. The cationic polyamines Spd and Spm are synthesized from Put by the successive and irreversible transfer of 2 aminopropyl groups from S-adenosylmethionine (Seiler, 1992). Polyamine synthesis is highly regulated by the action of 2 key enzymes, namely ornithine decarboxylase and S-adenosylmethionine decarboxylase, and polyamine acetylation and further oxidation allows interconversion for rapid changes in cellular concentrations (Seiler, 1987). Under TN conditions, dietary manipulation of amino acids may alter the metabolism of polyamines in birds. Bedford et al. (1987) observed increased kidney arginase activity in chickens, followed by increased renal ornithine and Put depositions after changing the Arg:Lys ratios through increasing Lys supplementation. Bedford et al. (1988) subsequently found that feeding ornithine increased the concentrations of ornithine, Put, and Spd in tissues in spite of reduced ornithine decarboxylase activity. Tissue concentrations of polyamines in birds seem to be particularly responsive to changes in dietary Arg, possibly due to the lack of a functional urea cycle (Smith, 1981). Furthermore, dietary Met has shown potential for affecting polyamine metabolism in chickens (Smith, 1981). To the authors’ knowledge, the effects of HS, Arg:Lys, and Met source on biogenic amines have not been studied in birds.
The present experiment was designed to investigate the effect of the Arg:Lys ratio and Met source interaction in heat-stressed chickens in terms of performance and its association to possible changes in duodenal and pancreatic polyamines.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) and raised in cages under TN conditions from 1 to 25 d of age. Birds were brooded under conventional management conditions, and then environmental temperature was gradually reduced to 19 to 20°C. Birds were cared for according to guidelines established by the University of Guelph’s Animal Care Committee. At that time, birds were randomized, and 12 replicates of 4 birds of similar weight were assigned to each experimental treatment that consisted of a 2 x 2 x 2 arrangement of environmental temperature, Arg:Lys, and Met source. Throughout the experimental period, birds were subjected to 1 of 2 environmental regimens, each replicated within 2 rooms. Broilers housed at 30.3 ± 1.0°C were regarded as heat stressed, and those kept at 19.1 ± 0.7°C were considered to be at thermoneutrality (Figure 1). At 30.3°C, birds were panting throughout the study. Temperature and RH were recorded hourly using 2 HOBO H8 loggers (Onset Computer Corporation, Bourne, MA) installed in all rooms. Birds were kept in cages (51 x 60 cm and 45-cm height) equipped with individual nipple drinkers and 51-cm feed troughs arranged in 2 tiers. Six experimental diets were prepared from a common basal diet adequate in all nutrients other than Arg. Free Arg was supplemented to achieve 2 ratios of Arg:Lys (0.85 and 1.40), and equimolar amounts of HMB or DLM were added to achieve requirement levels (Table 1). Amino acid analyses of the experimental diets were performed by the Experiment Station Chemical Laboratories (University of Missouri, Columbia) following the procedure no. 982.30 E (a,b,c) of the Association of Official Analytical Chemists (1995). Dietary concentrations of HMB were analyzed at Novus International Inc. (St. Charles, MO), using the method of Ontiveros et al. (1987). Mash diets and water were offered ad libitum. Feed intake (FI), BW gain (BWG), and efficacy for CP accretion (CPE) were ascertained at 33 and 47 d of age. Crude protein accretion was determined by comparison of body protein compositions of birds assayed at 26, 33, and 47 d of age. For calculation of CPE, 20 birds were killed by cervical dislocation at 26 d, and 1 bird per replicate cage was sampled at 33 and 47 d of age. Carcasses were frozen for subsequent determination of body fat and N. Dry homogenates from whole carcasses were obtained using the technique described by Sibbald and Fortin (1982), and N content was determined according to the Association of Official Analytical Chemists International Official Method 990.03. Dietary N content was assessed using the same technique.
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The pancreas and a second portion of approximately 10 cm of distal duodenum were also obtained at 33 and 47 d of age. These tissues were flushed gently with a 0.9% NaCl solution, submerged in dry ice, and kept at –80°C for further analysis. The concentrations of Put, Spd, and Spm were determined in these tissues as well as in all experimental diets. Samples were prepared and analyzed by HPLC, using gradient elution to separate the amines on an ALKION cation-exchange column (Varian Inc., Palo Alto, CA), followed by postcolumn derivitization and fluorescence following the technique detailed by Salazar et al. (2000). The procedures described herein were approved by the University of Guelph Animal Care Committee.
Statistical Analyses
Data from production parameters, VH, and tissue concentrations of polyamines were tested using the GLM procedure of SAS Institute (1998), according to the following equation
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where Yijklm = the mean of 4 birds (cage mean) obtained from the lth replicate fed a diet supplemented at the ith Arg:Lys ratio (0.85 or 1.40), the jth Met source (HMB or DLM) in birds under the kth temperature (HS or TN) housed in the mth room (room 1 and 2). Partial correlation coefficients were calculated within replicates of the same environmental treatment between the duodenal and pancreatic concentrations of Put, Spd, and Spm as dependent variables and the corresponding BWG, FI, efficiency of CPE, and VH of birds as independent variables.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Laboratory analyses confirmed that the dietary content of TSAA equivalents were in close agreement to formulation concentrations. Dietary concentrations of Put and Spd were similar across diets. Values for Spm were below detection levels (Table 1).
From 26 to 33 d of age, the environment and its interaction with dietary supplements had an effect on various dependent variables. During this period, the BWG, FI, and duodenal VH of birds was impaired by HS (Table 2; P < 0.01). An interaction between HS and Met source was also found for FI, such that birds on HMB ate more feed than did the DLM birds when housed under TN (P < 0.01), but not HS, conditions. This resulted in a tendency of the former group to gain more weight (P < 0.10) under TN conditions.
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Tissue concentrations of pancreatic and duodenal polyamines were affected by HS from 26 to 33 d (Table 2). A decline in Spd (P < 0.001) in both tissues was seen in heat-stressed birds, as well as a decrease in duodenal Put (P < 0.001). Independent of HS, the addition of Arg increased pancreatic Put and Spd (P < 0.001), and feeding DLM increased the concentrations of pancreatic Spm (P < 0.05). Duodenal Put also increased in birds fed DLM, but only in diets with high Arg:Lys (P < 0.05).
From 26 to 33 d at TN conditions, a positive correlation was found between feed consumption and duodenal Spm (P < 0.007), whereas negative correlations were observed between FI and duodenal Put (P < 0.03) and between VH and pancreatic Spd (P < 0.02; Table 3). Duodenal and pancreatic polyamines did not correlate with any dependent variable measured in birds under HS during this period (P > 0.05).
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). Environmental temperature affected most production parameters tested; BWG, FI, and CPE were impaired by HS. Interestingly, VH decreased with HS, although this was partially ameliorated by using an Arg:Lys of 1.40 (P < 0.01). High Arg diets increased the CPE (P < 0.01), but tended to depress FI in birds kept at TN conditions in addition to improving CPE in birds under HS (P = 0.06). When HMB was added to Arg-deficient diets for HS birds, poor CPE was observed. However, when Arg concentrations in the diet increased, optimum CPE was achieved by feeding HMB (Table 4).
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; P = 0.08) may be of particular relevance, given the fact that all production parameters correlated negatively with this metabolite (Table 5). Spermidine concentrations decreased under HS in both tissues tested (P < 0.001), but increased in duodenum when feeding a high-Arg diet only at TN conditions (P < 0.01). Pancreatic Put increased when feeding HMB (P < 0.05) and when heat-stressed birds were fed low-Arg diets (P < 0.05); however, neither Put nor Spd levels correlated with changes in performance (Table 5). There was a significant negative correlation between pancreatic Spm and BWG in heat-stressed birds (Figure 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). The same numerical trend was observed for FI during the second phase of the study (Table 4). The dietary additions of HMB and DLM were equimolar, and the concentrations of TSAA and HMB in the diets were in agreement with expected levels of supplementation (Table 1). The response of broilers to HMB relative to that of DLM has been a topic of considerable scientific debate for nearly 3 decades. In general, lower performance has been obtained in birds fed HMB in crystalline amino acid diets as compared with those with DLM (Motl et al., 2005), whereas similar performance has occurred when commercial-type diets are used (Daenner and Bessei, 2003). Furthermore, Vázquez-Añón et al. (2003), using sorghum-based diets, observed that optimum performance was achieved in broilers only when HMB was supplemented, whereas birds fed DLM had lower FI than the former group. These data imply that dietary conditions may change the response of chickens to dietary HMB relative to DLM when fed at requirement levels at TN conditions.
Brake et al. (1998) reported that, in the presence of equimolar amounts of Lys, the total intestinal uptake of Arg in vitro was negatively impaired, mainly due to a reduction in the Na-independent transport pathway. These researchers related their findings to improvements in the performance of heat-stressed birds when they were fed high Arg:Lys. From 34 to 47d of age, in line with the hypothesis that HS increases requirements for Arg, increasing dietary Arg tended to stimulate FI, but only in heat-stressed birds. The reduced VH caused by HS was partially ameliorated when feeding higher levels of Arg. This trend was nonsignificant from 26 to 33 d but was statistically significant from 34 to 47 d (P < 0.01; Table 4).
Mitchell and Carlisle (1992) and Uni et al. (2001) hypothesized that lower levels of plasma triiodothyronine, caused by HS, may be responsible for decreased villus mass, depressed enterocyte proliferation, and lower intestinal brush border membrane enzyme expression in chickens. However, vascular changes may also contribute to this effect, because the capillary blood flow to the gut is reduced considerably during hyperthermia, which may limit the flow of nutrients (Wolfenson et al., 1981; Wolfenson, 1986). Lower tissue concentrations of polyamines have been associated with reduced VH in calves and piglets fed isolated soybean proteins in milk replacers, whereas dietary supplements of Put partially ameliorates this effect under TN conditions (Grant et al., 1989, 1990). In the present trial, feeding higher levels of Arg tended to increase duodenal concentrations of Put independently of HS or Met source (P < 0.10). Although the partial correlations between VH and duodenal Put were not significant (P > 0.05), pancreatic concentrations of Spm correlated negatively with this parameter after 3 wk of HS, although increasing Arg did not affect pancreatic Spm levels (P > 0.05). Different Arg metabolites, such as nitric oxide, may have contributed to the beneficial effect of increasing Arg on the VH of hyperthermic birds (Balnave and Brake, 2002). The source of Met did not have an effect on VH in this study (P > 0.05).
From 34 to 47 d of age, birds fed diets high in Arg had greater BWG when fed HMB. However, when low-Arg diets were used, growth was optimized by feeding DLM (P < 0.10). This effect was independent of environmental temperature, except for CPE, whereas birds under HS had the lowest CPE when fed HMB in low-Arg diets, whereas optimum CPE was obtained for birds fed HMB in high-Arg diets (P < 0.10; Table 2). These observations agree with those of Balnave and Oliva (1990), who reported a lower FCR for chronically heat-stressed chickens fed HMB used in diets mildly deficient in Arg, compared with those fed DLM. Thus, under HS, using HMB rather than DLM in Arg-deficient diets may impair certain production parameters.
In the current trial, dietary Arg and Met source affected the tissue contents of duodenal and pancreatic Put, Spd, or both during both periods tested (Tables 2 and 4). In general, increasing Arg tended to increase tissue concentrations of polyamines, whereas changes in polyamine pools driven by Met sources showed no consistent trend and may be reflective of differences in uptake, tissue distribution, and metabolism among these Met sources (Saunderson, 1985, 1987; Dupuis et al., 1989; Lobley et al., 2001; Dibner 2003). Most of these changes were not related to changes in performance; thus, in spite of the close regulation of these metabolites, dietary manipulation may affect the pools of polyamines in various tissues without having profound effects on growth.
Most polyamine concentrations were affected by high temperatures. From 26 to 33 d of age, duodenal Put decreased in heat-stressed birds (P < 0.05), but pancreatic Put remained unaffected (P > 0.05). Pancreatic Put increased in hyperthermic chickens from 34 to 27 d of age (P < 0.01), whereas duodenal Put decreased (P < 0.001). Spermidine concentrations were consistently lower in both tissues at both ages during HS (P < 0.001; Tables 2 and 4). However, changes in Put or Spd were not associated with performance variables for broilers under HS at any time (P > 0.05), except for duodenal Spd, which was positively correlated to FI (P < 0.05). Reduced CPE, influenced by changes in the Arg:Lys and the source of Met, was followed closely by increases in pancreatic Spm only in heat-stressed chickens (Table 4).
Numerical changes in BWG followed the same trend, which resulted in a negative correlation between pancreatic Spm levels and all performance parameters tested in hyperthermic chickens (Table 5; Figure 2). Whether changes in pancreatic Spm had any influence on the interaction between Arg:Lys and Met source in hyperthermic broilers is unclear. The nuclear polyamine Spm is more toxic to chickens than Put or Spd (Sousadias and Smith 1995; Smith et al., 1996), and, consequently, tissue accumulation of Spm may have a greater effect than does change in Put or Spd in the heat-stressed chicken. Tissue accumulation does not occur after dietary supplementation of Spm, in spite of causing impaired growth. Its metabolite, N1-acetylspermine, a less cationic and less toxic compound, does accumulate in both the kidney and liver (Sousadias and Smith, 1995). It is well established that the toxic accumulation of polyamines is associated with cellular death and apoptosis (Poulin et al., 1995; Hu and Pegg, 1997). Certain conditions of cellular stress, such as hypotonic shock, lead to cytotoxic accumulation of polyamines and cellular death (Poulin et al., 1993). The association between pancreatic Spm and impaired performance, as in the context of the interaction between Arg:Lys and Met source, deserves further investigation.
In summary, data collected in this study with broilers indicate that changes in production parameters affected by HS are dependent on dietary Arg:Lys, Met source, or both. On the other hand, birds fed DLM were not affected by Arg level (P > 0.05). Dietary changes in Met source and Arg:Lys affect the duodenal and pancreatic contents of polyamines, although performance is unaffected. The effect of HS on the concentrations of duodenal and pancreatic polyamines was characterized by lower tissue Spd from 26 to 33 d and 34 to 47 d of age and higher pancreatic Spm, but only after prolonged HS, whereas changes in Put were inconsistent. Changes in the CPE of chronically stressed birds due to changes in dietary Arg:Lys and Met source closely followed those of pancreatic Spm, as were numerical differences in BWG, FI, FCR, and VH. The role of polyamine metabolism affecting the HS birds response to Arg:Lys and Met source warrants further attention. In chronically HS broilers, levels of pancreatic Spm were negatively associated with most performance characteristics. In retrospect, it would have been interesting to measure kidney levels of polyamines, because this is where most are detoxified. The pancreas is a major site of uptake of labeled Met (Novus Int., personal communications), and so any changes to this supply of Spm precursor could possibly contribute to Spm toxicity and, hence, alteration of performance. It would be interesting to study the incorporation of labeled Met into pancreatic and duodenal polyamines of heat-stressed broilers, and to concurrently study efficiency of detoxification in the kidney.
Received for publication December 14, 2005. Accepted for publication March 29, 2006.
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