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Poult Sci 2008. 87:276-283. doi:10.3382/ps.2007-00207
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METABOLISM AND NUTRITION

The Effects of Tomato Powder Supplementation on Performance and Lipid Peroxidation in Quail

N. Sahin*,1, C. Orhan*, M. Tuzcu{dagger}, K. Sahin* and O. Kucuk{ddagger}

* Department of Animal Nutrition, Faculty of Veterinary Science, and{dagger} Department of Biology, Faculty of Science, Firat University, 23119 Elazig, Turkey; and{ddagger} Barbara AnnKarmanos Cancer Institute, Wayne State University, Detroit, MI 48201

1 Corresponding author: nsahinkm{at}yahoo.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Recent studies have suggested a protective role for lycopene, an antioxidant carotenoid, in the prevention of stress including environmental stress. Tomatoes and tomato products are the major dietary source of lycopene. The objective of the present study was to investigate the effect of dietary tomato powder supplementation on the performance and lipid peroxidation of meat in Japanese quail (Coturnix coturnix japonica) exposed to a high ambient temperature of 34°C. A total of 180 ten-day-old male quails were randomly allocated into 6 groups consisting of 10 replicates of 3 birds. Birds were kept in wire cages in a temperature-controlled room at either 22°C (thermoneutral) or 34°C (heat stress) for 8 h/ d (0900 to 1700 h during the study). Birds were fed either a basal diet or the basal diet supplemented with 2.5 or 5.0% of tomato powder. Tomato powder supplementation linearly increased feed intake, live weight gain, and feed conversion (P = 0.01) under heat stress conditions but did not show the same effect at thermoneutral conditions (P > 0.05). Heat stress significantly increased malondialdehyde concentration and decreased vitamin concentrations in the serum, liver, and muscles of quail. Serum lycopene and vitamin C, E, and A (P = 0.01) concentrations increased linearly in birds at all groups. Malondialdehyde levels in serum, liver (P = 0.001), and muscles linearly decreased in all birds of both thermoneutral and heat stress groups as dietary tomato powder supplementation increased. The results of the study indicate that tomato powder modulates the oxidation-antioxidation system of the muscles in Japanese quail exposed to high ambient temperature.

Key Words: tomato powder • lipid peroxidation • malondialdehyde • stress • quail


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Stress factors such as high ambient temperature reduce feed intake, live weight gain, and digestibility of nutrients in poultry (Donkoh, 1989; Sahin and Kucuk, 2003). Heat stress (HS) causes the release of corticosterone and catecholamines and initiates lipid peroxidation in cell membranes (Edens and Siegel, 1975). Heat stress may exacerbate a marginal carotenoid deficiency or an increased carotenoid requirement (Sahin and Kucuk, 2003). Heat stress also increases lipid peroxidation, considered to be the major cause of quality deterioration in meat, meat products, and egg yolk (Pearson et al., 1983; Sahin et al., 2006b). The rate of lipid oxidation in meat also depends on the presence of prooxidants and antioxidants (Tichivangana and Morrissey, 1985; Ruiz et al., 1999). Carotenoids are the most important pigments for providing attractive colors in fruit and vegetables and may be found in all parts of the plant. Carotenoids have been described as excellent antioxidants because of their ability to quench singlet oxygen and trap peroxyl radicals (Burton and Ingold, 1984; Osterlie and Lerfall, 2005).

Several beneficial effects of some micronutrients known as antioxidants such as vitamin E, ascorbic acid, β-carotene, and lycopene have been reported (DiMascio et al., 1989; McDowell, 1989; Rao and Agarwal, 1999). Oxidative stability has been improved by antioxidant supplementation for foods of animal origin (Flachowsky, 2000; Flachowsky et al., 2002). Recent studies have shown that diets enriched with antioxidant substances could be used to attenuate the negative effects of environmental stress, which implies that detrimental effects of environmental stress could be partly consequent to induction of oxidative stress (Bollengier-Lee et al., 1998; Sahin and Kucuk, 2003). Tomato and tomato-based products contain some phytochemicals that may have health benefits and are important sources of many established nutrients. Lycopene, folate, vitamin C, vitamin A, phenolics, and flavonoids are potential bioactive compounds found in tomatoes (Beecher, 1998; Agarwal and Rao, 2000). Lycopene is a major carotenoid present in tomatoes and a highly potent antioxidant that provides protection against cellular damage caused by reactive oxygen species (DiMascio et al., 1989; Rao and Agarwal, 1999) and also is implicated as a potential cancer chemopreventive agent. Guo et al. (2001) reported that there is a significant inverse relationship between TBA reactive substances value in the thigh meat and egg and the dietary antioxidants. We have previously observed a preventive effect of lycopene on oxidative stress in the Japanese quail (Sahin et al., 2006a). However, nothing is known about the effects of tomato powder on the oxidative stress in stressed quail. The aim of this study was to evaluate the effects of dietary tomato powder as a source of lycopene on the performance and lipid peroxidation in Japanese quail exposed to thermoneutral and high ambient temperatures of 22 and 34°C, respectively.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Birds, Diets, Experimental Design, and Data Collection
A total of 180 ten-day-old male Japanese quail (Coturnix coturnix japonica) obtained from a commercial company (Insanay Kanatli Hayvan Uretim Paz. Tic. Inc., Elazig, Turkey) were used in the study. The experiment was conducted at the Veterinary Control and Research Institute of Elazig, Turkey. The birds were randomly assigned, according to a 2 (thermoneutral, TN) x 3 (powder levels: 0, 2.5, 5.0%) factorial design, to 6 treatment groups consisting of 10 replicates of 3 birds. There was no blocking criterion. Birds were kept in wire cages in a temperature-controlled room at either 22°C for 24 h/d (TN) or 22°C for 16 h/d and 34°C (HS) for 8 h/d (0900 to 1700 h). At both temperatures, birds were fed either a basal diet or the basal diet supplemented with 2.5 or 5.0 % tomato powder. Small amounts of the basal diet were first mixed with the respective amounts of tomato powder as a small batch and then mixed with a larger amount of the basal diet until the total amounts of the respective diets were homogenously mixed. Diets were stored in black plastic containers at 4°C to protect against oxidation. Food cups containing the diet were also protected from light. The birds were fed a starter diet until 21 d of age followed by a grower diet from d 21 to 42. Diets and fresh water were offered ad libitum. Light was provided continuously (24 h) throughout the experiment. Ingredients and chemical composition of the basal diet were shown in Table 1Go. The basal diets contained 22–20% (starter-grower) CP and 12.9 KJ/kg of ME. Feed intake and BW were determined at weekly intervals. Weight gain and feed conversion of birds were then calculated.


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  		Table 1. Composition of the experimental diets
 
Laboratory Analyses
For analyses in sera and tissues, at the end of study, 10 birds (1/replicate) randomly chosen from each treatment group were slaughtered, and blood samples were collected. Blood samples were centrifuged at 3,000 x g for 10 min, and sera were collected. Sera samples were kept on ice and protected from light until they were processed to prevent any artifactual oxidation during the experiments. The breast, leg, and liver were removed and vacuum packed in aluminum foil bags. Samples were stored at –80°C until analysis. Breast, leg, and liver sample malondialdehyde (MDA) levels were detected as mentioned previously by Sarraga et al. (2006) with HPLC (Shimadzu, Tokyo, Japan). Briefly, 3 g of sample was homogenized in 27 mL of 1.15% KCl. A 0.2-mL aliquot of the homogenate was mixed with 1 mL of 80 mM Tris-maleate buffer, pH 7.4; 0.4 mL of ascorbic acid and 0.4 mL of ferrous sulphate were added, and the mixture was incubated in a 37°C water bath. Then, 4 mL of 26 mM TBA, 0.92 M trichloroacetic acid, and 0. 8 mM HCl were added and held for 15 min in boiling water. The samples were cooled, and the absorbance was recorded at 532 nm. Serum MDA, vitamin C, vitamin A, and vitamin E concentrations were also measured by HPLC (Shimadzu) using Shimadzu UV-VIS SPD-10 AVP detector and a CTO-10 AS VP column. For MDA and vitamin C, the mobile phase was 30 mM KH2PO4-methanol (82.5 + 17.5, vol/vol %, pH 3.6), and the flow rate was 1.2 mL/min. Chromatograms were monitored at 250 nm, and injection volume was 20 µL (Karatepe, 2004). Serum vitamin A concentration was measured at 470 nm with a mobile phase of methanol and toluene (3:1; Tang and Huang, 1998). Serum vitamin E concentration was measured using a fluorescence detector with excitation at 288 nm and emission at 340 nm with a mobile phase of methanol and toluene (3:1; Cheng et al., 1999). Serum lycopene level was measured as described previously by Khachik et al. (1997, 2002). Chemical analyses of the diet samples were performed using procedures described by AOAC (1990) methods (988.05, 920.39, 962.09, 968.08).

Statistical Analyses
All parameters were analyzed using repeated measures analysis with PROC MIXED procedure of SAS (1999) for the effects of tomato powder, environment, and their interaction. Linear, quadratic, and cubic polynomial contrasts were used to evaluate effects of tomato powder levels (0, 2.5, 5.0%). Statistical significance was assumed at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Tomato powder was a sun-dried tomato product and contained 11% CP, 4.5% fat, 0.8 mg of lycopene, 0.13 mg of β-carotene, 1.73 mg of vitamin C, and 0.07 mg of (tocopherol per gram of powder. Table 2Go shows the effects of heat stress and tomato powder supplementation level on BW, feed intake, and feed conversion. Heat stress affected live weight, feed consumption, and feed conversion (P = 0.001). Birds kept in TN conditions had greater daily feed consumption and consumed a greater amount of feed per kilogram of live weight gain than hens kept in HS conditions. Body weight, feed intake, and feed conversion in birds kept at thermoneutral temperature were not affected by tomato powder supplementation. However, tomato powder supplementation linearly increased feed intake (P = 0.01), live weight gain (130 g vs. 121 g; P = 0.01), and feed conversion (P = 0.01) under stress conditions. Although BW gain and feed intake of birds did not differ by tomato powder doses in TN conditions, they increased with doses in HS conditions (P = 0.01, dose x heat interaction; Figure 1Go). There were also temperature x tomato powder level interaction effects on live weight gain, feed consumption, and feed conversion (P = 0.01). Tomato powder did not affect live weight and feed consumption for birds placed in TN conditions, whereas these variables for birds placed in HS conditions increased as supplemental tomato powder level increased (Table 2Go and Figure 1Go). The MDA levels in TN conditions were lower than HS conditions. In both conditions, dose was effective. The MDA levels in muscles, liver, and serum (0.65 vs. 0.07, 2.50 vs. 1.15, and 1.79 vs. 0.55; P = 0.001) linearly decreased in birds with dietary tomato powder supplementation in all birds of both TN and HS groups (Table 3Go and Figure 2Go). There were interaction effects of temperature and tomato powder levels on serum (P = 0.02) and breast and leg muscles and liver MDA concentrations (P = 0.001; Table 3Go and Figure 2Go). Serum concentrations of vitamins C, E, and A (P = 0.01) and total lycopene (17 vs. 0.0; P = 0.001) linearly increased in birds fed diets supplemented with tomato powder (Table 3Go and Figure 2Go). No detectable amount of lycopene was found in the serum of birds from the control group, whereas lycopene concentrations were higher in a dose-dependent fashion in the treatment groups. There were interaction effects of temperature and tomato powder levels on serum vitamins (P = 0.05) and lycopene (P = 0.001) concentrations (Table 3Go and Figure 3Go).


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  		Table 2. Effects of tomato powder supplementation on performance in Japanese quail reared under heat stress1
 

Figure 1
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  		Figure 1. The effects of temperature and tomato powder levels on performance in Japanese quail reared under heat stress on (a) live weight gain (P < 0.01), (b) feed intake (P < 0.01), and (c) feed conversion (P < 0.01). TN = thermoneutral; HS = heat stress; MDA = malondialdehyde.

 

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  		Table 3. Effects of tomato powder supplementation on lipid peroxidation and vitamin values in serum and tissues in Japanese quails reared under heat stress1
 

Figure 2
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  		Figure 2. The effects of temperature and tomato powder levels on lipid peroxidation in Japanese quail reared under heat stress on (a) breast (P < 0.001), (b) leg (P < 0.001), and (c) liver (P < 0.010). TN = thermoneutral; HS = heat stress; MDA = malondialdehyde.

 

Figure 3
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  		Figure 3. Effects of tomato powder supplementation on serum vitamin and lycopene values in Japanese quails reared under heat stress on (a) lycopene (P < 0.001), (b) vitamin C (P < 0.01), (c) vitamin E (P < 0.01), and (d) vitamin A (P < 0.01). TN = thermoneutral; HS = heat stress.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Heat stress has a major effect on the welfare and performance of poultry. Growth rate, feed intake, and feed efficiency decrease when ambient temperature goes above the thermoneutral zone (18 to 22°C). High environmental temperature induces a cascade of neural and hormonal events ending with an increase in production and release of corticosteroids, primarily corticosterone in birds (Siegel, 1995). Elevated concentrations of glucocorticoids exert catabolic effects, decrease the rate of synthesis, and thus result in muscle wasting and retardation in growth (Hayashi et al., 1992; Higuchi et al., 1996). We have previously reported increased performance of Japanese quail with pure lycopene supplementation (Sahin et al., 2006a). However, to our knowledge, this is the first study to be reported evaluating the effects of tomato powder supplementation on the performance and antioxidant status of quails. Tomato and tomato products contain some phytochemicals that may have health benefits and are important sources of many established nutrients. Epidemiological reports show a significant association between high intakes of tomatoes or tomato-based products and a reduced risk of cancer (Giovannucci et al., 1995; Kucuk, 2002). Therefore, there is increased interest in the antioxidant components present in tomatoes (e.g., lycopene, ascorbic acid, phenolics, and flavonoids; Abushita et al., 1997). Lycopene is the carotenoid with the highest concentration found in tomatoes and tomato products, and dietary intake of lycopene has been shown to have a biological effect in cancer (Kucuk et al., 2001, 2002). However, tomato also contains other carotenoids, including phytoene, phytofluene, and the provitamin A carotenoid β-carotene (Rao and Agarwal, 1999), which may have a synergistic effect with lycopene. In the present study, tomato powder supplementation had no significant effects on the measured values under thermoneutral conditions in growing Japanese quails; however, it improved the performance, namely live weight gain and feed conversion, and exerted positive effects on antioxidant components in quail reared under heat stress (34°C; Table 2 and 3GoGo, Figure 1Go). Growth retardation in stressed groups of the present study is probably due to decreased muscle protein synthesis and elevated proteolysis in muscle (Hayashi et al., 1994). The muscle proteolysis could be the result of damage of muscle proteins caused by active oxygen (Hunt et al., 1988), and this may be reversed by some antioxidants such as epigallocatechin gallate (Eid et al., 2003). It is not known yet whether lycopene has such an effect. Leal et al. (1999) reported that the broilers exposed to mycotoxins showed a decrease in BW, feed intake, and feed efficiency, and these decreases were partly alleviated by lycopene supplementation. Parallel to the results of the present study, Jain et al. (1999) reported that live weight and feed intake were not affected by lycopene supplementation in rats under thermoneutral conditions.

It has been reported that heat stress increases lipid peroxidation and depresses growth in birds (Sahin et al., 2003; Sahin and Kucuk, 2003). Lycopene, found in tomato and tomato powder is known to have an effective free radical scavenging activity (DiMascio et al., 1989), and this action could be beneficial to poultry, because hazardous free radicals are formed under stress, fast growth, high reproduction rates, and intensive metabolism conditions of poultry. Dietary supplementation with tomato products increased serum lycopene levels and reduced endogenous levels of oxidation of lipids, proteins, lipoproteins, and DNA (Agarwal and Rao, 1998; Porrini and Riso, 2000).

In the present study, tomato powder supplementation decreased MDA concentrations of serum, liver, and leg and breast muscles (Table 3Go and Figure 2Go). Malondialdehyde is one of the most frequently used indicators of lipid peroxidation associated with oxidative stress. Lipid peroxides and their products can cause damage to membrane-bound enzymes and other macromolecules, including DNA, and have been implicated in several disease processes (Halliwell and Gutteridge, 1988). Lipid oxidation of foods such as meat causes the formation of off-flavor; changes of taste, texture, and color; and loss of nutrients (Addis, 1990). The results of this study confirm that the daily consumption of small amounts of tomato products improves the status of antioxidant agents in the meat. Increase in these vitamins after supplementation with tomato powder suggests that the tomato powder is either the source of the vitamins or may protect the levels of these vitamins through its antioxidant effect (Agarwal and Rao, 2000). The effect of tomato powder on MDA levels found in our study confirms previously reported findings of other investigators (Jain et al., 1999; Rao and Shen, 2002). The decrease in oxidative stress observed in animals supplemented with tomato powder supports the hypothesis that compounds found in tomato powder might have a role in diminishing the stress effects by their antioxidant effect. Similar to our results, Jain et al. (1999) reported that dietary lycopene decreased serum TBA reactive substances (14% reduction) concentration in rats. Sahin et al. (2004, 2006a) reported that quail supplemented with pure lycopene had a significant reduction in MDA values in serum and liver.

It has been also reported that tomato product consumption can affect not only the lycopene status but also that of other antioxidant microconstituents such as β-carotene, lutein, and zeaxanthin (Tyssandier et al., 2004). In addition to the antioxidant effect, increased serum levels of β-carotene and vitamin A observed in the lycopene-supplemented groups may also have decreased lipid peroxidation levels. Furthermore, the tomato powder we used has significant amounts of vitamins C and E, which may have also contributed the observed effects in this study. The results of the present study in lipid peroxidation agree with previous studies in poultry meat (Renerre et al., 1999; Gatellier et al., 2000; Carreras et al., 2004; Sarraga et al., 2006). Similar to our results, Morrissey et al. (1996) reported that antioxidant supplementation of the diet resulted in increased antioxidant concentration such as vitamin E in poultry muscles.

In conclusion, tomato powder supplementation restored the heat stress-induced impairment in antioxidant status and reduced the negative effects of heat stress. Heat exposure decreased performance when the basal diet was fed. Tomato powder supplementation linearly increased feed intake, live weight gain, and feed conversion under stress conditions, and MDA levels in muscles, liver, and serum decreased in birds. The results of this study may also be applicable to prevention of cancer and cardiovascular diseases, which are associated with increased oxidative stress.

Received for publication May 27, 2007. Accepted for publication October 14, 2007.


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