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Poult Sci 2007. 86:1920-1926
© 2007 Poultry Science Association
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METABOLISM AND NUTRITION

Effect of Dietary Rhodobacter capsulatus on Cholesterol Concentration and Fatty Acid Composition in Broiler Meat

U. Salma*, A. G. Miah*, T. Maki{dagger}, M. Nishimura{dagger} and H. Tsujii*,1

* Laboratory of Animal Biotechnology, Interdisciplinary Graduate School of Science and Technology, Shinshu University, Minamiminowamura, Nagano 399-4598, Japan; and {dagger} Matsumoto Institute of Microorganisms Co. Ltd., 2904 Niimura, Matsumoto-city, Nagano 390-1241, Japan

1 Corresponding author: htsujii{at}gipmc.shinshu-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The study was designed to investigate the effects of dietary Rhodobacter capsulatus on cholesterol concentration and fatty acid composition in broiler meat. A total of 45 two-week-old male broiler chicks were randomly assigned into 3 treatment groups and fed ad libitum diets supplemented with 0 (control), 0.02, and 0.04% R. capsulatus for a 6-wk feeding period. The results of this study revealed that the supplementation of 0.04% R. capsulatus in diet reduced (P < 0.05) cholesterol and triglyceride concentrations in broiler meat. The concentrations (expressed as a percentage of total fatty acids) of oleic acid (18:1), linoleic acid (18:2), and linolenic (18:3) acid in thigh muscle and breast muscle were higher (P < 0.05) in the broilers fed the 0.04% R. capsulatus supplemented diet than in the broilers fed the control diet. The ratio of unsaturated fatty acids to saturated fatty acids was greater (P < 0.05) in both muscles of broilers fed the 0.04% R. capsulatus supplemented diet than the control diet. In addition, the concentrations of serum cholesterol and triglyceride, and hepatic cholesterol and triglyceride were also reduced (P < 0.05) by dietary R. capsulatus. Compared with the control diet, the 0.04% R. capsulatus supplemented diet reduced (P < 0.05) the ratio of low-density lipoprotein-cholesterol to high-density lipoprotein-cholesterol. Moreover, the supplementation of R. capsulatus in broiler diets did not show any adverse effect on production performance. Therefore, these results conclude that the application of R. capsulatus into diet may be feasible to reduce cholesterol concentration and improve the ratio of unsaturated fatty acids to saturated fatty acids in broiler meat.

Key Words: Rhodobacter capsulatus • broiler • cholesterol • fatty acid composition


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
There has been growing interest over recent years in the modulation of the cholesterol content and fatty acid composition in poultry products because occurrence of cardiovascular heart diseases are closely related to the dietary intake of cholesterol and saturated fatty acid (SFA) contents (Sacks, 2002). It is widely acknowledged that there is an urgent need to return to a balanced fatty acid diet by decreasing intake of cholesterol and saturated fats (Evans et al., 2002). Cholesterol content in chicken meat can be altered by varying the composition of diet, age, and gender (Wang et al., 2005). In recent years, research has been focused to reduce fat, cholesterol, and SFA contents of poultry meat by dietary supplementation of garlic (Konjufca et al., 1997), copper (Pesti and Bakalli, 1996), {alpha}-tocopherol acetate (Ashgar et al., 1989), and n-3 fatty acid (Ayerza et al., 2002). Several reports indicated that dietary supplementation of bacteria such as Lactobacillus cultures (Jin et al., 1998) reduced serum cholesterol in broilers; Rhodopseudomonas capsulatus (Lee et al., 1990) and Rhodopseudomonas palustris (Tsujii et al., 2007) reduced serum cholesterol concentration in rats. Our recent studies showed that cholesterol and triglyceride concentrations in serum of rats (Tsujii et al., 2007) and laying hens (Salma et al., 2007), as well as in egg-yolk (Salma et al., 2007) were markedly reduced by dietary Rhodobacter capsulatus. However, there is no study with the information regarding changes of cholesterol concentration and fatty acid composition in chicken meat by dietary R. capsulatus. Therefore, the present study was designed to investigate the effects of dietary supplementation of R. capsulatus on cholesterol and triglyceride concentrations, and fatty acid composition in broiler meat, as well as serum cholesterol and triglyceride concentrations.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Birds, Management, and Diets
A total of 60 newly hatched male Chunky broiler chicks were obtained from Mori Hatchery, Fukuoka, Japan. Chunky broiler is one of the most famous broiler strains developed in Japan and belongs to the Cornish line (Shen et al., 2002). The conditions and standards of care used in this study were in accordance with Guideline for Regulation of Animal Experimentation, Faculty of Agriculture, Shinshu University. The chicks were placed in a battery brooder and raised on a commercial starter diet until 2 wk of age. At 2 wk of age, 45 chicks with almost similar BW (370 to 375 g) were selected and randomly assigned into 3 treatment groups so that there were 15 chicks in each group. They were caged individually into wire-mesh cages (40 x 40 cm) with individual feed-trough and common water-trough. Room temperature was maintained at 20 to 24°C, and lighting was provided continuously throughout the experimental period. They were provided ad libitum drinking water and experimental diets for 6 wk. The basal diet was a commercial broiler finisher diet (Toyohashi Shiryo, Kabushiki Gaisha, Aichi, Japan), which was supplemented with 3 levels of R. capsulatus (on dry weight basis): 0 (control), 0.02, and 0.04%. The composition of the basal diet is shown in Table 1Go. The R. capsulatus was grown in outdoor culture under natural illumination as previously described method (Tsujii et al., 2007). Briefly, the cells of R. capsulatus were collected by centrifugation and spray-dried. The dried R. capsulatus powder was mixed with high soft mineral mix (MIM Co., Ltd., Matsumoto, Japan) as 1:10 and stored at 4°C. The nutrient composition of the dried R. capsulatus powder is shown in Table 2Go.


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  		Table 1. Composition of basal diet
 

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  		Table 2. Nutrient composition of Rhodobacter capsulatus1
 
Data Collection
The weights of the birds were recorded at beginning and end of the experimental period. During the experimental period, daily feed intake per bird and mortality were recorded. Feed conversion was calculated from BW gain and feed weight taken up to 6-wk experimental period.

Blood Collection
Blood sample from each individual broiler was collected at the end of the experimental period. Blood was collected from the brachial vein of overnight fasted broilers using sterilized syringes and needles. After 1 h standing at room temperature, serum was isolated by centrifugation at 1,000 x g for 10 min. Serum samples were stored at –80°C until analyzed.

Liver, Muscle, and Abdominal Fat Collection
At the end of the 6-wk feeding period, broilers were decapitated, and the weight of carcass and edible meat were recorded. Left liver lobe, left side thigh (biceps femoris), and breast (pectoralis major) muscles without skin and adipose tissues were collected from the same location and washed with normal saline, blotted dry on filter paper, chopped, ground, and stored at –20°C. Muscle was dissected free of surface (nonintrinsic) fat. Abdominal fat content was measured by removing and weighing all adipose tissues surrounding the gizzard, cloaca, and adjacent muscles (Kubena et al., 1974).

Liver and Muscle Sample Preparation
Total lipid in liver and muscle samples was extracted following the method described by Elkin and Rogler (1990). In briefly, about 1 g each of liver and muscle samples was homogenized with 12 mL of chloroform-methanol 2:1 (by volume) and filtered directly into a 50-mL volumetric flask using a glass microfiber filter. Following rehomogenization and refiltration, the liver and muscle filtrates were diluted to a final volume of 50 mL with chloroform-methanol 2:1 (by volume). In addition, to increase the concentration of lipid extract of the muscle samples, the chloroform-methanol was removed by rotary evaporator (Virtis, Gardiner, NY) following centrifugation (1,000 x g for 10 min) and filtration, and finally the dried extract was dissolved in 5 mL of chloroform-methanol 2:1 (by volume). The lipid extract samples were stored at –80°C until analyzed.

Enzymatic Analysis
Total cholesterol, triglyceride, and high-density lipoprotein (HDL) cholesterol concentrations in serum were determined enzymatically using commercially available reagent kits (Wako Pure Chemical Industries Ltd., Tokyo, Japan) as described in our previous study (Salma et al., 2007). Cholesterol and triglyceride concentrations in total lipid extracts obtained from liver and muscle (thigh and breast) samples were determined using the same reagent kits as those used for serum analysis.

Fatty Acid Determination
Total lipid extracts of muscle samples were transmethylated into fatty acid methyl esters and separated by using a gas chromatograph (Simadzu, GC14B, Kyoto, Japan). Aliquots of 2 µL were injected into an Omegawax 250 capillary column (30 m x 0.25 mm i.d.; 0.25-µm thickness; Supelco, Bellefonte, PA) with cyanopropyl methyl silicone as stationary phase. Helium was used as the carrier gas at a constant flow rate of 4.7 mL/min. The following oven temperature program was used: 100°C held for 1 min, increased to 160°C at 40°C/min, then to 240°C at 7°C/min, and 240°C held for 10 min. Peaks were separated using a flame-ionization detector and were quantified with an electric integrator (Shimadzu, CR-7A, Kyoto, Japan) using pure standard mixtures (Sigma, St. Louis, MO) and were identified. We adopted the weight percentage of each fatty acid in all detected fatty acids as a measurement value.

Statistical Analysis
Data were analyzed using the Fisher’s protected least significant difference test. The NCSS (Number Cruncher Statistical System, NCSS Statistical Software, Kaysville, UT) Version 5.01 computer software package was used for all statistical analysis. All data are expressed as means ± SEM. Differences were considered significant at the level of P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The effects of dietary R. capsulatus on cholesterol and triglyceride concentrations in muscle after the 6-wk feeding period are shown in Table 3Go. Cholesterol concentrations of thigh and breast muscle were significantly reduced in the broilers fed 0.04% R. capsulatus supplemented diet. Triglyceride concentrations in thigh and breast muscle of broilers were also significantly reduced by the 0.04% R. capsulatus supplemented diet. Compared with the control diet, the 0.02% R. capsulatus supplemented diet could not show any significant reduction of cholesterol and triglyceride concentrations in thigh or breast muscle. Hepatic cholesterol and triglyceride concentrations were lower in the broilers fed the 0.04% R. capsulatus supplemented diet than in the broilers fed the control diet.


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  		Table 3. Effect of dietary Rhodobacter capsulatus on liver weight, cholesterol and triglyceride concentration in liver, and thigh muscle (biceps femoris) and breast muscle (pectoralis major) of broilers after 6-wk feeding period1
 
The influences of dietary R. capsulatus on fatty acid composition in thigh and breast muscle after 6-wk feeding period are shown in Tables 4Go and 5Go. The concentrations of oleic acid (18:1), linoleic acid (18:2), and linolenic (18:3) acid in thigh muscle were significantly higher in the broilers fed 0.04% R. capsulatus supplemented diet than in the broilers fed the control diet. The concentrations of these fatty acids in breast muscle were also significantly increased by 0.04% R. capsulatus supplemented diet. Among the SFA, palmitic acid (C16:0) was significantly decreased by R. capsulatus (0.04%) supplemented diet in only thigh muscle, not in breast muscle. The R. capsulatus supplemented diets did not show any significant effect on stearic acid (C18:0) concentration in thigh or breast muscle. The concentration of monounsaturated fatty acid (MUFA) and polyunsaturated fatty acid (PUFA) were significantly increased in both muscles of broilers fed the 0.04% R. capsulatus supplemented diet compared with muscles of broilers fed the control diet. The ratio of PUFA/SFA or PUFA+MUFA/SFA was greater in thigh and breast muscle of broilers fed the 0.04% R. capsulatus supplemented diet than the control diet.


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  		Table 4. Effect of dietary Rhodobacter capsulatus on fatty acid composition (% of total fatty acids) in thigh muscle (Biceps femoris) of broilers after 6-wk feeding period1
 

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  		Table 5. Effect of dietary Rhodobacter capsulatus on fatty acid composition (% of total fatty acids) in breast muscle (pectoralis major) of broilers after 6-wk feeding period1
 
Total cholesterol, triglyceride, HDL cholesterol and low-density lipoprotein (LDL) cholesterol:HDL cholesterol concentrations in serum of the broilers fed diets supplemented with 0, 0.02, and 0.04% R. capsulatus for 6 wk are shown in Table 6Go. Compared with the control diet, serum cholesterol was significantly reduced in the broilers fed the 0.04% R. capsulatus supplemented diet. In comparison with the control diet, average concentration of serum triglyceride responded similarly in the broilers fed the 0.04% R. capsulatus supplemented diet. About 14 mg/dL of an increase in HDL cholesterol was achieved by 0.04% R. capsulatus supplemented diet than control diet. The ratio LDL cholesterol:HDL cholesterol was observed significantly lower in broilers fed the 0.04% R. capsulatus supplemented diet than the other diets.


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  		Table 6. Effect of dietary Rhodobacter capsulatus on total cholesterol, triglyceride, low-density lipoprotein (LDL) cholesterol, high-density lipoprotein (HDL) cholesterol, and LDL cholesterol:HDL cholesterol in serum of broilers after 6-wk feeding period1
 
After 6-wk feeding period, BW gain, feed intake, feed conversion, and abdominal fat content in the broilers fed diets supplemented with 0, 0.02, and 0.04% R. capsulatus are shown in Table 7Go. Body weight gain, feed intake, and feed conversion were not significantly different among the broilers fed the R. capsulatus supplemented diets or the control diet. The average content of abdominal fat in the broilers was significantly decreased by the 0.04% R. capsulatus supplemented diet than the control diet. Mortality was 0% in all groups during the experimental period.


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  		Table 7. Effect of dietary Rhodobacter capsulatus on body weight gain, feed intake, feed conversion, and abdominal fat content in broilers after 6-wk feeding period1
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The modulation of the fatty acid composition of poultry meat by dietary means is relatively easy, but the reduction of cholesterol concentration is more difficult (Skrivan et al., 2000). However, the present study demonstrated that the cholesterol concentration in broiler meat was reduced by dietary R. capsulatus. Other studies also reported that copper supplements in excess of the nutritional requirement lowered muscle cholesterol (Bakalli et al., 1995; Konjufca et al., 1997). Shim et al. (2004) observed that feeding Codonopsis lanceolata root reduced meat cholesterol. In the present study, the opportunity of this greater reduction of cholesterol concentration in thigh muscle was possibly due to the presence of higher cholesterol concentration in thigh muscle than in breast muscle. A possible explanation was drawn by Konjufca et al. (1997) that meat cholesterol concentration is usually associated with total fat content of the tissue, which is more abundant in thigh than in breast muscle.

The present study revealed that the dietary R. capsulatus could alter the composition of fatty acids in broiler meat. Tsujii et al. (2007) observed that addition of R. capsulatus into the rat diet altered the fatty acid composition in serum. In this study, the ratio between the diversified unsaturated fatty acids (UFA) and SFA were increased in the broiler meat by supplementation of R. capsulatus in diet. High contents of MUFA in animal products may be beneficial for human health. Several nutritional studies strongly support a relationship between SFA and the risk of cardiovascular heart diseases, and hence there is a need to reduce consumption of SFA and increase consumption of PUFA. Dietary R. capsulatus (0.04%) improved the ratio of PUFA and SFA in thigh and breast muscle and brought it more in line with the 1:1 ratio that was recommended for human consumption (Canada Health and Welfare, 1990; American Heart Association, 1991). Dietary SFA are an independent risk factor associated with cardiovascular heart diseases; their negative effects on LDL cholesterol are stronger than the effects of dietary cholesterol (American Heart Association, 1988; Hornstra et al., 1998). Pinchasov and Nir (1992) reported that the increase of PUFA reduced the synthesis of monoenoic fatty acids through inhibiting the activity of the 9-desaturase complex. The 9-desaturase complex introduces monoenoic fatty acids into the liver lipids, thereby facilitating their incorporation into VLDL cholesterol and their transport to abdominal adipose tissue (Donaldson and Mueller, 1971; Wahle, 1974; Jeffcoat, 1979; Legrand et al., 1987).

Observations made in the present study reveal that cholesterol concentration in thigh and breast muscle of the broilers has a positive correlation with the change of the cholesterol contents in serum. In this study, supplementation of R. capsulatus into the broiler diet was shown to reduce serum cholesterol concentration. This reduction is similar to our previous studies conducted in rats (Tsujii et al., 2007) and in laying hens (Salma et al., 2007) by feeding with R. capsulatus supplemented diets. Lee et al. (1990) observed that dietary supplementation of Rhodopseudomonas capsulatus also reduced serum cholesterol in rats. Therefore, the present results are in agreement with our previous results and confirmed that dietary R. capsulatus was able to reduce not only cholesterol but also triglyceride concentration in serum.

Deposits of fat in the abdominal area of the broilers are considered as a waste for poultry. Not only is abdominal fat a loss, but it also represents an added expense for the processing effluent treatment in further processing. Our study revealed that this type of waste by the poultry industry could be reduced through deposition of lower fat content in abdominal area of the broiler by R. capsulatus supplementation in diet.

The cholesterol lowering and other beneficiary effects of R. capsulatus demonstrate in this study are not clearly understood. However, we speculated that carotenoids are the most important key factor present in the R. capsulatus stimulated in decreasing serum cholesterol through acting as hypocholesterolemic agents. Amen and Lachance (1974) reported that beta-carotene and canthaxanthin have a hypocholesterolemic effect in rats, and beta-carotene seems to displace cholesterol in the transport of lipoproteins. Moreover, R. capsulatus is not only rich in carotenoids, but also in protein contents, amino acids (lysine, arginine, glycine etc.), vitamins (riboflavin, B6, folic acid, C, E, etc.) as well as minerals (Mg, Mn, Fe, Cu, etc.; Table 1Go); most of them were demonstrated to be cholesterol-lowering factors in several studies. One attractive explanation for the cholesterol-lowering effect of R. capsulatus involves the specific combination and higher concentration of amino acids. The R. capsulatus is an excellent source of arginine (3.34%), glycine (2.41%), and lysine (2.86%), which were reported as hypocholesterolemic agents (Vahouny et al., 1984). Kritchevsky et al. (1982) proposed a relationship between the lysine to arginine ratios of intact protein as a factor involved in the regulation of hypercholesterolemia. Vitamin E is known as a cholesterol-lowering factor (Phonpanichrasamee et al., 1990). Besides these, among the minerals present in R. capsulatus, Cu (Bakalli et al., 1995) and Mg (Ouchi et al., 1990) have the ability to lower serum cholesterol.

In view of dietary health, food that contains more UFA and relatively lower cholesterol contents can help in reducing the occurrence of cardiovascular heart diseases. We found that not only the serum cholesterol and triglyceride, but also the meat cholesterol and triglyceride concentrations were reduced by supplementation of R. capsulatus to the broiler diet. The R. capsulatus-supplemented diet improved the ratio UFA:SFA by altering the fatty acid composition in muscle. Moreover, the supplementation of R. capsulatus in broiler diets did not show any adverse effect on production performance. Therefore, these results led to the conclusion that the application of dietary R. capsulatus into diet may be feasible to reduce cholesterol concentration and improve the ratio of UFA to SFA in broiler meat.

Received for publication November 19, 2006. Accepted for publication April 24, 2007.


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 ABSTRACT
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 RESULTS
 DISCUSSION
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