Nutritional Factors Affecting Abdominal Fat Deposition in Poultry: A Review

Nutrient levels on abdominal fat

Fat types on abdominal fat

Fats and oils are used in poultry diet formulations to enhance the palatability of the diet, the absorption of fat-soluble vitamins, and to regulate the passage rate of the digesta in the gastrointestinal tract. They are also the most concentrated sources of energy (Baião and Lara, 2005). In avian species, the amount of fat that accumulates in the body depends on the available plasma lipid substrate, which originates from the diet or de novo lipogenesis in the liver (Hermier, 1997). Therefore, the sources of lipids in poultry diets may affect their total body fat deposition. Sanz et al. (1999; 2000a) observed that a diet containing tallow or lard (saturated fat) achieved the same growth performance as a diet that contained sunflower oil (unsaturated fat), whereas the abdominal fat content was significantly lower in the chickens fed diets containing sunflower oil. Experimental evidence indicated that dietary inclusion of sunflower oil was effective for reducing total body fat deposition compared with a diet containing tallow, but this raised the question of why the inclusion of unsaturated fats in the diets of broiler chickens led to a lower accumulation of body fat compared with the inclusion of saturated fats. However, Sanz et al. (2000b) found that the inclusion of sunflower oil in the diet of broilers led to a significant reduction in the abdominal fat percentage by inhibiting the activity FAS in the liver and enhancing the activities of CPT I and L3HOAD in the heart compared with the inclusion of tallow in the diet. Therefore, unsaturated fats reduce abdominal fat deposition and total body fat via this mechanism, in contrast to saturated fats. However, the next question was whether all unsaturated fats reduce abdominal fat deposition in broiler chickens. Therefore, Crespo and Esteve-Garcia (2001; 2002a) fed chickens diets supplemented with tallow (a rich source of saturated fatty acids), olive oil (a rich source of monounsaturated fatty acids), sunflower oil (a rich source of n-6 type polyunsaturated fatty acids), and linseed oil (a rich source of n-3 type polyunsaturated fatty acids). They reported that chickens fed diets supplemented with sunflower or linseed oils had a significant reduced in abdominal fat percentage and other fat depots, including mesenteric and neck fat, compared with chickens fed diets supplemented with tallow or olive oil. According to the results of Sanz et al. (2000b), the inclusion of sunflower oil in the diets of broilers promoted fatty acid oxidation and depressed fatty acid synthesis, so the abdominal fat percentage was decreased significantly. Linseed oil is a source of n-3 type polyunsaturated fatty acids while sunflower oil contains n-6 type polyunsaturated fatty acids. Thus, linseed oil could have reduced total body fat via the same mechanism as sunflower oil or other mechanisms. However, Crespo and Esteve-Garcia (2002b) found that inclusion of linseed oil in the diets of broilers led to a significant reduction in the abdominal fat percentage and a significant increase in fatty acid synthesis compared with tallow or sunflower oil, so linseed oil may reduce the abdominal fat percentage by elevating fatty acid β-oxidation. A similar result was reported by Newman et al. (2002) who found that, compared with the addition of tallow, the addition of sunflower or fish oil to the diets of broilers from 21 to 56 days of age reduced abdominal fat deposition, increased the consumption of oxygen, and decreased the rate of oxygen consumption relative to the rate of carbon dioxide production, which showed that polyunsaturated fatty acids activate fatty acid β-oxidation. Furthermore, Ferrini et al. (2010) reported that, compared with those fed diets containing tallow, the activity of L3HOAD increased significantly whereas the activities of MDH and G-6-PDH (lipogenic enzymes) did not change in chickens fed diets containing linseed oil. This showed that linseed oil reduces abdominal fat deposition by promoting fatty acid β-oxidation, rather than suppressing fatty acid biosynthesis. Therefore, polyunsaturated fatty acids (n-3 and n-6 types) that have many benefits for human health (Simopoulos, 2000) can be used during poultry production to rear poultry products containing the optimal ratio of polyunsaturated fatty acids (n-3 and n-6) but also to reduce fat deposition in the abdomen area of poultry, which will enhance the producer returns and consumer health.

Conjugated linoleic acid on abdominal fat

The source of oils is not the only factor that can affect abdominal fat deposition in broilers. The structure of oil (fatty acid isomers) is one of the most important factors that can affect body fat deposition in broilers, as demonstrated by Simon et al. (2000). Their results indicated that the inclusion of conjugated linoleic acid (CLA) in chicken diets reduced the skin fat (one of the most important fat depots in poultry) compared with diets that lacked linoleic acid. CLA is a common name for the positional and geometric isomers of linoleic acid (9cis, 12cis octadecadienoic acid; 18:2n 6). A similar result was also reported by Badinga et al. (2003) who found that CLA depressed fat deposition in the livers of chickens in a comparison of CLA and corn oil (a rich source of linoleic acid). Moreover, Szymczyk et al. (2001) showed clearly that the inclusion of 1.5% CLA in broiler diets significantly reduced the abdominal fat content compared with the control diet (0% CLA). CLA can reduce abdominal fat deposition and lower total carcass fat deposition, as reported by Du and Ahn (2002). Zhang et al. (2009a) also supplemented 2.5% CLA in the diet of geese, which resulted in a significant reduction in the abdominal fat content compared with supplementation with the same amount of soybean oil, which is a rich source of linoleic acid. Zhang et al. (2007) and Zhou (2008) showed that CLA reduced body fat deposition in unimproved chicken strains (local strains), which have a low capacity for synthesizing lipids compared with improved strains (modern commercial chickens), as demonstrated by Cui et al. (2012). Zhang et al. (2007) demonstrated that a Beijingyou chicken diet containing 1.0% CLA led to a significant reduction in the abdominal fat content compared with a control diet that contained corn oil. The abdominal fat deposition was reduced significantly by adding 3.0% CLA to the diets of Yellow-feather broiler chickens compared with control diets containing 3.0% rapeseed oil as a rich source of linoleic acid (Zhou, 2008). According to these studies, CLA is a new tool that can be used to reduce fatness in modern broiler chickens, although the question remains why the inclusion of CLA in broiler diets caused a significant reduction in the abdominal fat content and total body fat deposition. Zhang et al. (2007) suggested that CLA reduces total body fat deposition in broilers by suppressing the activity of LPL in the plasma, while Zhou (2008) suggested that CLA reduced abdominal fat deposition in Yellow-feather broiler chickens (local Chinese strain) by downregulating peroxisome proliferator-activated receptor γ (PPARγ) mRNA expression in abdominal adipose tissue. Royan et al. (2011) confirmed the findings of Zhou (2008) by testing the inclusion of CLA in the diet of a commercial strain of broiler chickens (Ross 308), which caused a significant reduction in the abdominal fat percentage by reducing PPARγ mRNA expression in the abdominal adipose tissue. In avian species, PPARγ, which regulates lipid metabolism and adipocyte differentiation, is strongly associated with abdominal fat deposition (Sato et al., 2009; Wang et al., 2008; Xiong et al., 2010). In geese, Zhang et al. (2009a) suggested that CLA reduces the abdominal fat pad percentage by activating fatty acid oxidation via an increase in the activity of CPT I. In avian species, we can conclude that CLA reduces total body fat deposition directly by reducing the activity of LPL and downregulating PPARγ mRNA expression, and indirectly by elevating the activity of CPT I.

Various feed additives on abdominal fat

Betaine (glycine betaine or trimethylglycine) is highly concentrated in sugar beet and is classified as a byproduct of sugar production. It is considered to be an important source for methyl donors in farm animals (Virtanen, 1995). In White Pekin ducks, Wang et al. (2004) detected a reduction in the abdominal fat yield percentage after the inclusion of betaine in their diet. Zhan et al. (2006) also found that adding betaine to a methionine-deficient diet significantly reduced the fat deposition in broiler chickens. Su et al. (2009) reported that feeding Landes geese a diet supplemented with betaine caused a significant decrease in the abdominal fat compared with a nonsupplemented group. Furthermore, Xing et al. (2011) obtained the same result using broiler chickens fed a diet supplemented with betaine. The fat-lowering effect of betaine was elucidated by Zhan et al. (2006) and Xing et al. (2011) who showed that betaine lowered the body fat content in broilers by increasing the activity of HSL and reducing the activities of FAS and LPL in the abdominal fat.

L-Carnitine, which transports long-chain fatty acids across the inner mitichondrial membrane during β-oxidation (the first step in fatty acid oxidation: catabolism), is a water soluble zwitterionic compound, which is synthesized in vivo from lysine and methionine (Golzar Adabi et al., 2011). Because of its role in transporting long-chain fatty acids across the inner mitichondrial membrane during β-oxidation, it appears that L-carnitine may play an important role in reducing fat deposition in modern strains of broiler chickens. Rabie and Szilagyi (1998) reported that the inclusion of L-carnitine in broiler diets at 50 mg/kg for five weeks from 18 to 53 days of age caused a significant reduction in abdominal fat deposition. Arslan et al. (2003, 2004) found that feeding Turkish native ducks and geese the same diet supplemented with 200 or 100 mg L-carnitine in drinking water, respectively, led to a reduction in the abdominal fat percentage. Xu et al. (2003) showed that the abdominal fat expressed as a percentage of live weight was significantly reduced by the addition of 50 mg/kg L-carnitine to the diets of broiler chickens. Feeding female broiler breeders a diet supplemented with 25 mg/kg L-carnitine also reduced the carcass fatness of their progeny (Kidd et al., 2005). Therefore, dietary L-carnitine supplementation decreases abdominal fat deposition in meat-type poultry by reducing the activities of G-6-PDH, MDH (lipogenic enzymes), and LPL in the abdominal fat, as suggested by Xu et al. (2003).

Probiotics is a name given to live microorganisms that have a positive effect on animal health. Santoso et al. (1995) indicated that probiotics can be added to broiler diets to reduce body fat deposition and carcass cholesterol, which suggests that probiotics beneficially regulate lipid metabolism. To test the findings of Santoso et al. (1995), Kalavathy et al. (2003) investigated the effects of Lactobacillus cultures on the abdominal fat traits and lipid profiles of broiler chickens. They found that feeding chickens aged 14 to 42 days on diets supplemented with a mixture of 12 Lactobacillus strains at 0.1% significantly reduced the serum triglyceride concentration, with a concomitant decrease in abdominal fat traits. Homma and Shinohara (2004) also reported that the inclusion of probiotic Bacillus cereus toyoi in the diets of male quails from 27 to 55 days of age for four weeks significantly reduced abdominal fat accumulation. Kalavathy et al. (2006) found that Lactobacillus cultures reduced the abdominal fat traits and also improved the carcass quality by reducing carcass fatness. Similarly, Yamamoto et al. (2007) showed that dietary supplementation with Aspergillus awamori-fermented distillery by-product, at 1.0% significantly lowered abdominal fat deposition in broiler chickens. Cao et al. (2012) found that feeding broiler chickens a diet supplemented with Aspergillus niger-fermented Ginkgo biloba leaves at 0.5% and 1.0% in the starter and grower phases, respectively, significantly reduced abdominal fat accumulation. Thus, Saleh et al. (2012) examined the effects of including Aspergillus awamori at 0.05% or 0.20% on abdominal fat deposition. They found that the inclusion of Aspergillus awamori at 0.05% was sufficient to induce a significant reduction in the abdominal fat percentage. In a comparison of the effects of Aspergillus awamori and Aspergillus niger on abdominal fat traits in chickens, Saleh et al. (2011) showed that Aspergillus awamori at 0.01% or Aspergillus niger at 0.05% in the diet significantly reduced abdominal fat deposition. Therefore, the deposition of poultry abdominal fat could be reduced by supplementing probiotics in the diet because probiotics inhibit lipid biosynthesis (Santoso et al., 1995; Yamamoto et al., 2007) and promote fatty acid catabolism (Homma and Shinohara, 2004).

Polysavone is extracted from alfalfa and contains 18.63% polysaccharides, 5.58% triterpenoid saponins, and 5.89% flavonoids. It has been implicated in the reduction of poultry abdominal fat deposition by downregulating the activity levels of ACC and FAS (Dong et al., 2007; Deng et al., 2012).

Green tea contains high levels of polyphenols, which are thought to be useful as antiobesity compounds. It has been reported that the inclusion of green tea powder at 0.5% in the diets of broiler chickens significantly reduced abdominal fat traits by inhibiting hepatic lipogenesis (Biswas and Wakit, 2001).

Chitooligosaccharide, which has a low molecular weight, low viscosity, and acceptable solubility, is an oligosaccharide that can be added to the diets of broiler chickens at 0.4% to reduce abdominal fat deposition (Zhou et al., 2009). Chitooligosaccharide lowered body fat deposition by reducing lipid uptake via the suppression of the enzyme activity of pancreatic lipase (Kang et al., 2012).

Chitosan is a linear polysaccharide with low viscosity that is produced commercially from crab and shrimp shell waste. Chitosan has been used to reduce the fat content in the abdominal area of poultry by inhibiting the absorption of dietary fat via the suppression of lipase activity due to a reduction in the levels of bile acids (Kobayashi and Itoh, 1991; Kobayashi et al., 2002).

Ginseng, the root of Panax ginseng C. A. Meyer, is a well-known traditional herbal drug in East Asian countries, which has been used to treat several heart diseases and metabolic diseases (Yan et al., 2011a). Ginseng has many bioactive components such as saponins that inhibit lipogenesis in chickens (Qureshi et al., 1983). The blood triglyceride concentration was significantly reduced by adding wild ginseng adventitious root to the diets of laying hens (Yan et al., 2011a). This reduced the availability of blood triglyceride for transport and deposition in the abdominal areas of poultry. Yan et al. (2011b) showed that the inclusion of wild ginseng adventitious root meal at 0.3% in the diets of broiler chickens led to a significant reduction in abdominal fat deposition.

Thyme (Thymus vulgaris) is a medicinal herb that can be used as a natural alternative to antibiotics in poultry production (Khan et al., 2012) but it also has inhibitory effects on abdominal fat traits in broiler chickens (Al-Kassie, 2009; Abdulkarimi et al., 2011). Al-Kassie (2009) showed that adding 200 ppm thyme oil to the diets of broiler chickens during the fatting period (42 days) caused a significant reduction in the abdominal fat percentage compared with the control diet. Abdulkarimi et al. (2011) reported that adding 0.6% thyme extract to drinking water significantly reduced the accumulation of fat in the abdominal areas of broiler chickens. The reduction in the abdominal fat traits caused by thyme supplementation may have been attributable to the saponins in thyme (Abdulkarimi et al., 2011), which have inhibitory effects on lipogenesis (Qureshi et al., 1983).

Dihydropyridine, which has been approved as an antioxidant in poultry feed (Bakutis and Bukis, 1984; Zou et al., 2007; Niu et al., 2010; 2011), can reduce abdominal fat traits in laying hens, broiler chickens, and broiler breeder hens (Zou et al., 2007; Niu et al., 2010; 2011). Zou et al. (2007) found that feeding laying hens a diet supplemented with 300 mg/kg dihydropyridine for three months significantly reduced abdominal fat deposition by increasing the activity of HSL in the abdominal fat. Niu et al. (2010) found that adding 100 mg/kg dihydropyridine to broiler diets from one to 42 days of age was sufficient to suppress the activities of LPL in abdominal fat, as well as MDH and G-6-PDH in the liver, and to increase the levels of HSL in abdominal fat, thereby reducing the abdominal fat percentage. In broiler breeder hens, Niu et al. (2011) showed that the inclusion of dihydropyridine at 200 mg/kg in the diet was sufficient to reduce the accumulation of fat in the abdomen area by simulating the activity of HSL in the abdominal fat.

Alpha lipoic acid is a naturally occurring compound that has beneficial effects on poultry production. Experimental evidence in poultry suggests that dietary alpha lipoic acid supplementation alleviates oxidative stress, enhances the antioxidant capacity, improves meat quality, and lowers body fat deposition (Zhang et al., 2009b; Chen et al., 2011; Halici et al., 2012; El-Senousey et al., 2013). Zhang et al. (2009b) reported that diets supplemented with 900 mg/kg alpha lipoic acid from one to 42 days of age reduced the abdominal fat content in broiler chickens. A similar result was reported by El-Senousey et al. (2013) who fed broiler chickens from 21 to 42 days of age using a diet supplemented with 800 mg/kg alpha lipoic acid. The fat-lowering effect of alpha lipoic acid may have been due to increased fatty acid β-oxidation (Shen et al., 2007) and/or elevated HSL activity (Fernandez-Galilea et al., 2012).

Feed restriction on abdominal fat

Limiting the feed intake in avian species using various methods (quantitative or qualitative feed restriction) has successfully addressed many problems that affect poultry farms due to intensive selection, e.g., fatness. Plavnik and Hurwitz (1985; 1991) showed that quantitative feed restriction was effective for reducing the abdominal fat content compared with full feeding. Santoso et al. (1993) also showed that quantitative feed restriction for 10 days (beginning on the first day in the second week of age for female broiler chickens) led to a significant reduction in the abdominal fat percentage and total body fat deposition. It is well known that female broiler chickens tend to deposit more fat than male broiler chickens. Moreover, Tan and Othani (2000) demonstrated that quantitative (50% of full feed) or qualitative (diet diluted with 50% rice hulls) feed restriction in White Pekin ducks for six days starting at eight days of age caused a significant reduction in body fat deposition at the end of the fatting period compared with full feeding. Rezaei et al. (2010) and Wu et al. (2012) confirmed that qualitative feed restriction in modern broiler chickens and meat-type ducks reduced body fat deposition. Rezaei et al. (2010) found that the inclusion of rice hulls in the diet of broiler chickens at a level of 20% for five days starting at 16 days of age significantly reduced the abdominal fat and total body fat deposition. Wu et al. (2012) showed that meat-type ducks fed a diet diluted with 40% rice hulls for seven days starting at eight days of age led to a significant improvement in the meat quality by reducing the fat depots, including abdominal fat and skin fat. In broiler chickens, Santoso (2001) found there was a significant depression in the abdominal fat percentage and in the accumulation of fat in the body at market weight by limiting the feed intake to 25% of the ad libitum level for nine days starting on the first day of the second week of age, in a comparison of different levels of feed restriction and full feed. Similarly, Chen et al. (2012) showed that feeding chickens a diet containing 70% of their energy requirements by limiting the feed consumption to 80% of the full feed significantly reduced the abdominal fat pad and the thickness of subcutaneous fat compared with the control.

Restricted feed consumption lowered the body fat content in meat-type chickens and ducks and also reduced fat accumulation in broiler breeders (Richards et al., 2003). Several studies have tested why feed restriction reduces the body fat content in poultry (Santoso et al., 1993; Tan and Othani, 2000; Yang et al., 2010; Wu et al., 2012). Santoso et al. (1993) suggested that quantitative feed restriction reduces fat deposition by inhibiting the activity of the rate-limiting enzyme during lipogenesis (ACC) in the livers of broiler chickens. Tan and Othani (2000) found that quantitative or qualitative feed restriction decreased the activities of the main lipogenic enzymes, including ACC and FAS, in the livers of White Pekin ducks. Wu et al. (2012) confirmed that feed restriction lowered the body fat content by decreasing the hepatic activity of MDH, G-6-PDH, and FAS enzymes. Santoso et al. (1993), Tan and Othani (2000), and Wu et al. (2012) confirmed the study of Zhong et al. (1995) who showed that feed restriction significantly reduced hepatic lipogenesis (in an in vitro study). Yang et al. (2010) suggested that feed restriction regulates body fat deposition to promote lean meat production by reducing fatty acid biosynthesis and elevating fatty acid β-oxidation. Therefore, feed restriction reduces fat deposition by inhibiting hepatic lipogenesis and elevating fatty acid oxidation. Zhong et al. (1995) found that early feed restriction significant reduced abdominal fat deposition because of a significant decrease in the number of abdominal adipose cells. Thus, the application of quantitative or qualitative feed restriction in commercial farms could be an effective method for reducing the level of undesirable fat in modern strains of poultry.