Fat Deposition in Broiler Chickens Offered Reduced-Crude Protein Diets

The development of reduced-crude protein (CP) diets for broiler chickens holds several potential advantages including reduced dependency on imported soybean meal by the Australian chicken-meat industry. Typically, reduced-CP diets contain less soybean meal but more feed grain (and starch) and more synthetic/crystalline amino acids. However, reducing dietary CP from 200 to 150 g/kg in isoenergetic diets has been shown to depress body weight gain, impair food conversion efficiency and increase heat production and abdominal fat deposition (Buyse et al., 1992). The purpose of this paper is to consider fat deposition in relation to starch overload or ‘carbotoxicity’ in poultry offered reduced-CP diets.

In humans, ‘carbotoxicity’ has been described as a condition where mono-, di- and polysaccharides undermine health by promoting obesity, diabetes and metabolic syndrome (Kroemer et al., 2018). Metabolic syndrome is a combination of obesity, dyslipidemia, hepatic steatosis, elevated blood glucose and hypertension (Glimcher and Lee, 2009). Starch, which is absorbed as glucose, is the main energy source in broiler diets; the majority of which is provided by the feed grain on which the diet is based. Plasma glucose levels in broiler chickens are high compared to mammalian species (Braun and Sweazea, 2008). However, post-prandial plasma glucose levels in birds offered maize-, wheat- or rice–based diets did not vary depending on starch source (P > 0.35) with an overall mean concentration of 12.72 mmol/L in Li et al. (2019). Thus, glucose homeostasis is maintained in poultry, despite relatively high plasma glucose levels. The metabolic disposal of glucose involves direct oxidation in various tissues, glycogen synthesis in liver and skeletal muscles and hepatic de novo lipogenesis (Jequier, 1994). Glucose can be stored as glycogen but massive carbohydrate overfeeding, or starch overload, in humans has been shown to trigger substantial de novo lipogenesis once glycogen stores in liver and skeletal muscle have been saturated (Acheson et al., 1988). Moreover, there are limited glycogen stores in muscle in avian species such as English sparrows (Braun and Sweazea, 2008). The liver is the main site of de novo lipogenesis in avian species, rather than adipose tissue. Glucose is catabolised to acetyl-CoA which is converted into fatty acids and cholesterol. Cholesterol and triacylglycerol are incorporated into very low density lipoproteins and transported to adipose and other tissues via the circulation (Wang et al., 2017). Thus, de novo lipogenesis is a complex metabolic pathway in which excess carbohydrate is converted into fatty acids that are then esterified to storage triacylglycerols (Ameer et al., 2014).

Increased fat deposition in broilers offered reduced-CP diets essentially stems from starch overload. In a series of three similar studies (Chrystal et al., 2020a,b,c), broiler chickens were offered maize-based diets with analysed dietary starch concentrations ranging from 303 to 448 g/kg, which were inversely related to crude protein concentrations that ranged from 215 to 155 g/kg. Collectively, dietary starch inclusions quadratically increased relative abdominal fat-pad weights. Estimates of carcass fat can be deduced by multiplying fat-pad weights by a factor of 4.83 (Du and Ahn, 2002). On this basis, increasing dietary starch levels quadratically increased total carcass fat (r = 0.678; P < 0.005), as shown in Figure 1.

Curiously, birds offered 165 g/kg CP, maize-based diets clearly outperformed their wheat-based counterparts by 53.0% (2370 versus 1549 g/bird) in weight gain and 19.9% (1.473 versus 1.840) in FCR, but had 71% heavier abdominal fat-pad weights (12.8 versus 7.5 g/kg) in Chrystal et al. (2021). In a subsequent (as yet unpublished) study, birds offered 175 g/kg CP, sorghum-based diets outperformed their wheat-based counterparts by 6.08% in weight gain and by 4.90% in FCR, but had 42% heavier fat-pads (12.2 versus 8.6 g/kg). Therefore, the starch properties of a given feed grain appear to have a tangible bearing on fat deposition in broilers offered reduced-CP diets and maize and sorghum are more likely to promote fat deposition than wheat. This is a conundrum in that while wheat is less likely to promote fat deposition, is not as likely to support acceptable growth performance in comparison to maize or sorghum in the context of reduced-CP diets.

It becomes relevant that wheat starch (0.036/minute) is digested at a faster rate than starch in maize (0.017/minute) or sorghum (0.018/minute) and the proportion of rapidly digestible starch in wheat (29.5%) is higher than in maize (20.9%) or sorghum (16.2%) under in vitro conditions (Giuberti et al., 2012). Importantly, these relationships appear to translate in vivo as the wheat starch digestion rate (0.117/minute) was more rapid than maize (0.087/minute) and sorghum (0.075/minute) in broilers offered nutritionally-equivalent, standard diets in Selle et al. (2021). Instructively, Ells et al. (2005) concluded that rapidly versus slowly digestible starch provoke distinctly different postprandial metabolic patterns in humans. Indeed, Seal et al. (2003) reported substantial differences in the incremental area under the curve (IAUC) for glucose and insulin in healthy humans in response to rapidly or slowly digestible starch. Rapidly digestible starch triggered an increase in IAUC of glucose by 53% and insulin by 91%. Thus, as reviewed by Lehmann and Robin (2007), rapidly digestible starch generates greater and more rapid changes in blood glucose, insulin and non-esterified fatty acid concentrations than slowly digestible starch. The extent to which these human outcomes apply to poultry is problematic given the inherent differences in the starch-glucose-insulin axes of avian and mammalian species (Tesseraud et al., 2007). Nevertheless, it is possible that sustained glucose and insulin blood levels generated by sorghum and maize-based diets is promoting more de novo lipogenesis than in birds offered rapidly digestible starch. It may be that glucose derived from rapidly digestible wheat starch is being more readily catabolised to generate energy either in the gut mucosa and/or post-enterally; whereas, glucose from slowly digestible starch is being converted to glycogen and then fat via de novo lipogenesis to greater extents.

Dietary starch:protein ratios are reflected in starch:protein disappearance rate ratios in broilers and, in turn, expanding disappearance rate ratios are associated with greater fat deposition. This is clearly illustrated by the quadratic relationship (r = 0.729; P < 0.001) between analysed dietary starch:protein ratios and relative abdominal fat-pad weights in broiler chickens as shown in Figure 2. Fairly obviously, one way to address the problem of increased fat deposition would be to limit or cap dietary starch:protein ratios in reduced-CP diets. This approach was evaluated in an initial study and displayed some promise (Greenhalgh et al., 2020). A second (as yet unpublished) study has been completed in which starch:protein ratios were condensed by 15% in maize-based diets, which was facilitated by substituting soybean meal with full-fat soy, sourced from the same producer (Soon Soon Oilmills Sdn Bhd). As shown in Table 1, condensing the dietary ratio from 2.76 to 2.35 in 175 g/kg CP diets improved weight gain by 3.45% (2398 versus 2318 g/bird), FCR by 3.75% (1.360 versus 1.413) with a marginal reduction in fat-pad weights from 12.78 to 11.47 g/kg.

Thus, the approach of capping dietary starch:protein ratios does hold promise but the real challenge will be to replace soybean meal with feedstuffs of lesser protein contents without compromising growth performance. In Australia, the obvious alternative is canola meal but the extent to which this feedstuff can be included in reduced-CP diets at the expense of soybean meal and remain feasible has yet to be investigated. Also, if importance of starch digestion rates is verified, it may be that reduced-CP diets based on sorghum-wheat blends will provide a more favourable, intermediate rate of starch digestion which will ameliorate fat deposition. Clearly, these two strategies are not mutually exclusive and could be evaluated in tandem. Thus, in conclusion, the development of reduced-CP broiler diets in Australia could be facilitated by capping starch:protein ratios coupled with diets based on appropriate wheat-sorghum blends to generate more favourable starch digestion rates.