Abstract
Objective
This study was conducted to assess the effect of potassium humate and enzymes (Xylanase+Amylase+Protease) inclusion in diets on carcass characteristics, meat quality and fatty acid profiles of broilers fed canola-based diets.
Methods
Two hundred and twenty broilers randomly allotted to 5 dietary treatments: the control (commercial broiler diet); CM (17.5% canola meal inclusion); CMEnz (17.5% CM inclusion+0.3 g/kg Axtra XAP); CMPh (17.5% CM inclusion+1.5% Potassium Humate, PH); and CMEnzPh (17.5% CM inclusion+1.5% PH+0.3 g/kg Axtra XAP) were slaughtered at day 42 for assessment of carcass and meat quality parameters.
Results
Diet had no effect on carcass traits apart from breast muscle weight and breast muscle index. The highest breast muscle weight was observed in broilers fed CMEnz (487.6±17.5 g) followed by those fed the control diet (474.37±17.5 g). Diet also had no significant dietary effect on pH, temperature, drip loss and shear force values of the breast muscle. However, diet significantly affected meat colour and water-holding capacity. Broilers in the control and CMPh groups (52.94±0.67 and 52.91±0.67) had the highest (p<0.05) values for lightness (L*), whilst those fed CMEnzPh had the lowest value (47.94±0.67). In contrast, CM group had the lowest (p<0.05) value for redness (a*) with CMEnzPh group having the highest values. The proportion of polyunsaturated fatty acids (PUFAs), n-6 and n-3 fatty acids and the PUFA/saturated fatty acid ratio were increased in CM-based diets containing enzymes and humic acid.
Conclusion
It can, therefore, be concluded that CM can be included in broiler diets in the presence of enzymes and humic acid with positive effects on meat quality and important fatty acids that are beneficial to the health of consumers.
Keywords: Canola, Humic Acid, Enzymes, Meat Quality, Fatty Acids
INTRODUCTION
Meat and meat products with higher levels of minerals (iron, zinc, and selenium), polyunsaturated fatty acids (PUFAs) and antioxidants are attractive and valued worldwide [1]. Presently, the production and consumption of chicken meat and its products has significantly increased worldwide due to desirable nutritional characteristics. In comparison to beef and pork, chicken products contain high amounts of protein, low fat content and relatively high concentrations of PUFAs, which are beneficial to the health of consumers [2]. Generally, nutrition of the chicken plays a significant role in influencing the composition of meat. The reported health benefits PUFAs in meat products has created a trend towards increasing the content of these fatty acids, particularly the omega 3 PUFAs, in meat through dietary manipulation [1,3].
High value protein sources used in broiler diets, including soybean meal (SBM) are becoming expensive due to the competition between humans and livestock for food and feed. This has provoked intense efforts to explore alternative protein sources that include canola meal (CM). Canola has crude protein levels that range from 34% to 39% and has comparable amino acid profile to that of SBM. Its use in broiler diets can, however, be limited by high fibre content, which may influence digesta viscosity and decrease nutrient availability [4,5]. Inclusion of enzymes and organics acids such as humic acids have been observed to improve digestibility of poor protein sources such as CM. In several studies, digestibility, efficiency of feed utilisation and meat quality of broilers was improved when a xylanase, amylase and protease enzyme complex was added to the broiler diet [1,6–8]. More important, xylanase has been observed to enhance disruption of cell wall material in canola, thus releasing captured carbohydrates while amylase may increase the digestion of the released carbohydrates [4]. On the other hand, protease might break down a portion of protein that may escape digestion in the gut ultimately increasing protein digestion efficiency [4,9]. It can, therefore, be expected that the inclusion of different combinations of enzymes in broiler diets can be a strategy to improve the nutritional value of CM and, consequently, alter the composition of meat.
Information regarding the influence of humic acids, a natural feed additive, on the digestion and utilisation of poor protein sources such as CM in broilers is scarce. Humic acid is a natural organic acid and has been shown to influence digestion, immune response and general performance of broilers [10]. Its inclusion in broiler diets may stimulate changes in digestion dynamics, assimilation of nutrients and meat metabolite profiling, resulting in desirable meat compositional and organoleptic physiognomic quality [1]. In chicken and pork, humic acid inclusion in diets was observed to desirably modify meat colour mainly due to accelerated myoglobin synthesis [10–12]. Moreover, in pork, humic acid was observed to have an effect of increasing the fat marbling values and to reduce back fat thickness, probably due its influence on protein and lipid distribution [12]. To our knowledge, no study has been conducted to evaluate the influence of humic acid on meat quality and fatty acid profiles in broilers fed poor protein sources such as CM. Therefore, the current study was designed to determine the effects of dietary humic acid and enzymes on carcass characteristics, meat quality and fatty acid parameters in broilers fed canola-based diets.
MATERIALS AND METHODS
Experimental design and diets
A total of two hundred and twenty birds (Cobb 500) from a feeding trial were used in the study. All chickens were given broiler starter mash from day 1 to 14. At the beginning of the grower phase (d 15), the birds were randomly allotted to 5 dietary treatments replicated 4 times with a pen housing 11 birds as the experimental unit. The study was arranged in a completely randomized design. The pens (measuring 3.5×1.0×1.85 m) were designed to meet the animal welfare standards for optimum production of broilers. Five dietary treatments in form of mash were formulated with the control diet being composed of a commercial grower diet whose major protein source was SBM, whilst the other four diets contained CM at 17.5% inclusion in place of SBM. The dietary treatments were formulated as follows: i) Control (commercial broiler diet); ii) CM (17.5% canola meal inclusion); iii) CMEnz (CM+0.3 g/kg Axtra XAP); iv) CMPh (CM+1.5% Potassium Humate, PH); v) CMEnzPh (CM+1.5% PH+0.3g/kg Axtra XAP). The 17.5% Canola inclusion was the maximum rate allowable for formulation of a balanced broiler diet, whilst the inclusion level of enzymes (Xylanase, Amylase, and Protease [g], Axtra XAP, OPTIFEEDS, Lichtenburg, South Africa) was the recommended level provided by feed companies for ingredients such as Canola, which are poor protein sources containing high fibre. Humic acid was added in the form of a humic acid salt (potassium humate, PH, NUTRICO, Johannesburg, South Africa). The inclusion level of humic acid was derived based on the ranges from literature [10,13].
Ingredients and dietary formulations are shown in Table 1 whilst Table 2 shows the nutritional compositions of the diets. Near-infrared reflectance spectroscopy was used to determine the proximate composition of the diets. The experimental diets were only offered during the grower (d 15 to 28) and finisher (d 29 to 42) phases. At the end of the feeding trial (d 42), all broilers were deprived of feed for a period of 13 hours to allow the clearing of the crop and subsequently slaughtered for assessment of carcass traits, meat quality and fatty acid profiles. All the study procedures were conducted at the North-West University experimental farm. The experimental procedures were approved by the Animal Research Ethics Committee of North-West University and the Ethics number granted is NWU-00516-16-S9.
Table 1.
Ingredients | Dietary treatments1) | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
| ||||||||||
Grower | Finisher | |||||||||
|
|
|||||||||
Control | CM | CMEnz | CMPh | CMEnzPh | Control | CM | CMEnz | CMPh | CMEnzPh | |
Yellow maize-fine | 69.90 | 69.50 | 69.50 | 69.50 | 69.50 | 76.20 | 76.40 | 76.40 | 76.40 | 76.4 |
Canola oilcake (HEX) | 0.00 | 17.50 | 17.50 | 17.50 | 17.50 | 0.00 | 17.50 | 17.50 | 17.50 | 17.50 |
Prime gluten 60 (Yellow) | 1.80 | 2.40 | 2.40 | 2.40 | 2.40 | 1.27 | 1.80 | 1.80 | 1.80 | 1.80 |
Fullfat soya | 5.10 | 5.10 | 5.10 | 5.10 | 5.10 | 1.53 | 1.61 | 1.60 | 1.59 | 1.54 |
Soybean meal (Local) | 19.70 | 2.22 | 2.21 | 2.22 | 2.22 | 18.00 | 0.50 | 0.60 | 0.50 | 0.50 |
Limestone powder-fine | 1.45 | 1.22 | 1.22 | 1.22 | 1.22 | 1.30 | 1.07 | 1.07 | 1.07 | 1.07 |
MCP/Mono Cal KK | 0.72 | 0.56 | 0.56 | 0.56 | 0.56 | 0.50 | 0.33 | 0.33 | 0.33 | 0.33 |
Salt-fine | 0.32 | 0.32 | 0.32 | 0.32 | 0.32 | 0.33 | 0.33 | 0.33 | 0.33 | 0.33 |
Bicarbonate | 0.17 | 0.16 | 0.16 | 0.16 | 0.16 | 0.13 | 0.12 | 0.12 | 0.12 | 0.12 |
Choline powder | 0.08 | 0.08 | 0.08 | 0.08 | 0.08 | 0.08 | 0.08 | 0.08 | 0.08 | 0.08 |
Lysine | 0.28 | 0.29 | 0.29 | 0.29 | 0.29 | 0.26 | 0.27 | 0.27 | 0.27 | 0.27 |
L-threonine | 0.04 | 0.00 | 0.00 | 0.00 | 0.00 | 0.03 | 0.00 | 0.00 | 0.00 | 0.00 |
Methionine | 0.19 | 0.18 | 0.18 | 0.18 | 0.18 | 0.16 | 0.09 | 0.09 | 0.09 | 0.09 |
PX P2 Br Gr with Phytase | 0.17 | 0.17 | 0.17 | 0.17 | 0.17 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 |
PX P3 Br Fin with Phytase | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.17 | 0.17 | 0.17 | 0.17 | 0.17 |
Coxistac | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 |
Olaquindox | 0.04 | 0.04 | 0.04 | 0.04 | 0.04 | 0.04 | 0.04 | 0.04 | 0.04 | 0.04 |
Axtra XAP (g/kg) | 0.00 | 0.00 | 0.30 | 0.00 | 0.30 | 0.00 | 0.00 | 0.30 | 0.00 | 0.30 |
Potassium humate (%) | 0.00 | 0.00 | 0.00 | 1.50 | 1.50 | 0.00 | 0.00 | 0.00 | 1.50 | 1.50 |
Dietary treatments: Control, commercial broiler diet; CM, commercial broiler diet in which 17.5% of soybean meal was replaced by canola meal; CMEnz, CM diet+0.3 g/kg Axtra XAP enzyme complex; CMPh, CM diet+1.5% potassium humate; and CMEnzPh, CM diet+1.5% PH+0.3 g/kg Axtra XAP enzyme complex.
Table 2.
Parameters | Standard broiler diet composition | Canola oil cake diet composition | ||
---|---|---|---|---|
|
|
|||
Grower | Finisher | Grower | Finisher | |
Volume | 100 | 100 | 100 | 100 |
Moisture | 10.93 | 11.27 | 11.34 | 11.57 |
Metabolizable energy (MJ/kg) | 11.79 | 11.9 | 12.09 | 12.29 |
Protein | 18.93 | 16.89 | 18.80 | 16.90 |
Fat | 6.24 | 6.38 | 5.96 | 5.99 |
Fibre | 4.17 | 4.02 | 4.31 | 4.20 |
Ash | 4.84 | 4.25 | 4.81 | 4.21 |
Linoleic | 2.97 | 2.52 | 2.96 | 2.55 |
Choline (mg/kg) | 1,285 | 1,159 | 1,283 | 1,173 |
Calcium | 0.85 | 0.75 | 0.85 | 0.75 |
Phosphorus | 0.56 | 0.50 | 0.59 | 0.49 |
Sodium | 0.18 | 0.16 | 0.17 | 0.17 |
Chlorine | 0.3 | 0.29 | 0.29 | 0.3 |
Potassium | 0.73 | 0.65 | 0.76 | 0.68 |
Arginine | 1.10 | 0.95 | 1.10 | 0.95 |
Carcass traits and internal organs
At slaughter, the birds were electrically stunned, exsanguinated, defeathered and eviscerated in accordance with the standard procedures for humane animal slaughter. The carcasses were weighed and packed in labelled plastics bags for each treatment. The internal organs (including the gizzards, livers, hearts, spleens, and intestines) were removed and packaged separately in labelled plastics bags and weighed individually. Lengths of small intestines (jejunum, duodenum, and ileum) were also measured individually and recorded. The hot carcass weight of each chicken was recorded and dressing out percentage was calculated. The carcasses were then chilled overnight, reweighed to obtain the cold carcass weight and thereafter the breast and thigh samples were obtained and weighed to determine the breast muscle and thigh muscle weights and ratios. Breast muscles were also obtained for the evaluation of meat quality traits and fatty acid profiles.
Meat quality measurement
Meat pH (pHu) and temperature measurements were taken 24 hours post-slaughter on the breast muscle (central area of the breast) using a Corning Model 4 pH-temperature meter (Corning Glass Works, Medfield, MA, USA). Colour of the meat (ΔL* = lightness, Δa* = redness, and Δb* = yellowness) was measured using a Minolta colour-guide (Spectrophotometer CM 2500c, Konika Minolta, Osaka, Japan). The water holding capacity (WHC) was determined as the amount of water expressed from fresh meat held under pressure (60 kg pressure) using the filter-paper press. Drip loss was determined as the difference in weight of meat sample suspended in bottle and stored in a cold room at 4°C for 72 hours before and after drip. The meat cooking loss was calculated as the difference between the weight of raw meat and cooked meat while meat tenderness was determined using a Meullenet - Owens Razor Shear Blade (A/MORS) mounted on a Texture analyser (TA XT plus, Stable Micro Systems, Surrey, UK). The reported value in Newtons (N) represented the average of the peak force measurements of each sample.
Fatty acid analysis
Total lipids of feed (Table 3) and muscle samples were quantitatively extracted, according to the method of Folch et al [14] using chloroform and methanol in a ratio of 2:1, while fatty acid methyl esters (FAMEs) were quantified using Varian 430 flame ionization gas chromatography, with a fused silica capillary column, Chrompack CPSIL 88 (100 m length, 0.25 mm ID, 0.2 μm film thicknesses) according to the procedures described by Aldai et al [15] and Alfaia et al [16]. Standards for identification of the FAMEs were obtained from Sigma-Aldrich (Aston Manor, Pretoria, South Africa) while all other reagents and solvents were of analytical grade were attained from Merck Chemicals, (Halfway House, Johannesburg, South Africa). Individual fatty acids were calculated as a proportion of total fatty acids present in the sample, while total fatty acids combinations were calculated as: omega-3 (n-3) fatty acids, omega-6 (n-6) fatty acids, total saturated fatty acids (SFA), total monounsaturated fatty acids (MUFA), PUFA, PUFA/SFA ratio, and n-6/n-3 ratio.
Table 3.
Parameter | Dietary treatments1) | SEM | ||||
---|---|---|---|---|---|---|
| ||||||
Control | CM | CMEnz | CMPh | CMEnzPh | ||
Total SFA | 20.57a | 15.28b | 14.91b | 15.1b | 15.1b | 0.14 |
Total MUFA | 31.67b | 32.06a | 32.01a | 31.75ab | 31.76ab | 0.10 |
Total PUFA | 47.76b | 52.66a | 53.07a | 53.17a | 53.16a | 0.23 |
Total n-6 | 46.06b | 48.29a | 48.52a | 48.72a | 48.69a | 0.16 |
Total n-3 | 1.72b | 4.37b | 4.55a | 4.45a | 4.48a | 0.21 |
PUFA:SFA | 2.33b | 3.45a | 3.56a | 3.52a | 3.53a | 0.13 |
n-6/n-3 | 26.77a | 11.07b | 10.67b | 10.96b | 10.88b | 0.10 |
SEM, standard error of the mean; SFA, total saturated fatty acids; MUFA, total mono unsaturated fatty acids; PUFA, total poly unsaturated fatty acids; n-6, total omega-6 fatty acids; n-3, total omega-3 fatty acids.
Dietary treatments: Control, commercial broiler diet; CM, 17.5% CM inclusion; CMEnz, 17.5% CM inclusion+0.3 g/kg Axtra XAP; CMPh, 17.5% CM inclusion+1.5% Potassium Humate; CMEnzPh, 17.5% CM inclusion+1.5% PH+0.3 g/kg Axtra XAP.
Means in the same row with different superscripts are significantly different (p<0.05).
Statistical analysis
Data on carcass characteristics, meat quality parameters and fatty acid profiles of broiler meat were analysed using general linear model procedure of SAS [17]. The statistical model was as follows:
Where: Yij = observation (carcass characteristics, meat quality parameters and fatty acid profiles), μ = population mean constant common to all observations, Ti = effect of diet, and ɛij = random error term. The probability differences (PDIFF) option of SAS [17] was used to perform pairwise comparisons and for all tests, the level of significance was set at (p< 0.05).
RESULTS
Carcass traits and internal organs
Results from the study showed a significant effect of diet on the breast muscle weight and breast muscle ratio (Table 4). The breast muscle weight and the ratio are indicative of muscle mass in a carcass. The highest breast muscle weight was observed in chickens offered CMEnz (487.6±17.5 g) diet followed by chickens fed CMPh (474.37±17.5 g). The CM fed broilers had the lowest breast weight. Similarly, CMEnz broilers had the highest breast muscle ratio followed by the CMPh. The CM fed broilers had the lowest breast muscle ratio. The weights of the internal organs (gizzard, heart, spleen) and intestinal length (duodenum, jejunum, ileum) were significantly (p<0.05) influenced by the diets (Table 5). The gizzard and spleen of broilers in the CMEnzPh treatment were heavier (p<0.05) than in broilers offered CMEnz. Chickens fed the CMEnzPh diet also had the longest jejunum followed by CMPh. The heart weight was heaviest (p<0.05) in CMEnz (25.90 g) whilst CMPh and CMEnzPh chickens had the lowest heart weights.
Table 4.
Parameters | Dietary treatments1) | SEM | ||||
---|---|---|---|---|---|---|
| ||||||
Control | CM | CMEnz | CMPh | CMEnzPh | ||
Final body weight (g) | 2,585 | 2,507 | 2,574 | 2,605 | 2,630 | 74.94 |
Hot carcass weight (g) | 1,806.25 | 1,870 | 1,915.25 | 1,970 | 1,963.75 | 106.19 |
Cold carcass weight (g) | 1,753 | 1,799.25 | 1,893.50 | 1,899.75 | 1,889.25 | 46.09 |
Dressing % | 69.92 | 69.02 | 72.05 | 75.52 | 74.64 | 4.42 |
Av Breast weight (g) | 422.82b | 383c | 487.6a | 474.37a | 487a | 17.5 |
Av Thigh weight (g) | 264.10 | 254.06 | 277.61 | 269.79 | 277.06 | 7.48 |
Breast muscle ratio | 0.22b | 0.23b | 0.27a | 0.26a | 0.26a | 0.01 |
Thigh muscle ratio | 0.15 | 0.15 | 0.15 | 0.14 | 0.15 | 0.01 |
SEM, standard error of the mean.
Dietary treatments: Control, commercial broiler diet; CM, 17.5% CM inclusion; CMEnz, 17.5% CM inclusion+0.3 g/kg Axtra XAP; CMPh, 17.5% CM inclusion+1.5% Potassium Humate; CMEnzPh, 17.5% CM inclusion+1.5% PH+0.3 g/kg Axtra XAP.
Means in the same rows with different superscripts are significantly different (p<0.05).
Table 5.
Parameters | Dietary treatments1) | SEM | ||||
---|---|---|---|---|---|---|
| ||||||
Control | CM | CMEnz | CMPh | CMEnzPh | ||
Gizzard (g) | 30.75c | 30.90c | 27.70d | 33.10b | 35.15a | 1.06 |
Heart (g) | 12.6b | 13.55a | 12.6b | 11.70c | 11.52c | 0.21 |
Spleen (g) | 2.45d | 2.35d | 2.85c | 4.15b | 4.69a | 0.18 |
Duodenum (cm) | 38.54a | 31.24c | 36.36b | 35.81b | 36.20b | 2.69 |
Jejunum (cm) | 41.28c | 35.28d | 45.10b | 44.80b | 47.64a | 4.87 |
Ileum (cm) | 52.34a | 41.70b | 53.68a | 42.74b | 43.34b | 3.66 |
Liver (g) | 41.55 | 42.85 | 42.69 | 40.65 | 40.00 | 1.27 |
HIS | 0.023 | 0.024 | 0.023 | 0.023 | 0.022 | 0.01 |
SEM, standard error of the mean; HIS, hepatosomatic index.
Dietary treatments: Control, commercial broiler diet; CM, 17.5% CM inclusion; CMEnz, 17.5% CM inclusion+0.3 g/kg Axtra XAP; CMPh, 17.5% CM inclusion+1.5% Potassium Humate; CMEnzPh, 17.5% CM inclusion+1.5% PH+0.3 g/kg Axtra XAP.
Means in the same rows with different superscripts are significantly different (p<0.05).
Meat quality
The results on meat quality measurements showed that diet only affected meat colour and WHC (Table 6). The findings of the current study, show an increase in redness (Δa*) with the inclusion of enzymes in the diets. However, broilers fed the Control and CMPh diets had lighter (ΔL*) breast muscles. Meat of broilers fed the control diet had the lowest water loss, which means it has the greatest capacity to retain water, whilst the meat of broilers supplemented with CMEnz showed the least capacity to retain water. In the current study, the effect of diet on shear force values was insignificant.
Table 6.
Parameters | Dietary treatments1) | SEM | ||||
---|---|---|---|---|---|---|
| ||||||
Control | CM | CMEnz | CMPh | CMEnzPh | ||
Ultimate pH | 6.12 | 6.16 | 6.12 | 5.95 | 5.89 | 0.09 |
Ultimate temperature (°C) | 14.63 | 12.56 | 14.08 | 15.54 | 16.69 | 0.69 |
Meat colour | ||||||
ΔL* | 52.94a | 50.79b | 51.35ab | 52.94a | 47.94c | 0.67 |
Δa* | 1.81c | 1.59d | 2.46b | 1.81c | 3.42a | 0.41 |
Δb* | 13.91b | 13.33b | 13.69b | 14.30a | 13.71b | 0.69 |
Water holding capacity (%) | 29.34c | 33.62b | 37.47a | 34.97b | 33.04b | 1.93 |
Drip loss (%) | 9.58 | 8.45 | 9.69 | 10.91 | 9.22 | 1.02 |
Cooking loss (%) | 13.75 | 14.73 | 18.07 | 14.45 | 12.40 | 1.47 |
Shear force (N) | 6.47 | 6.38 | 8.32 | 8.81 | 8.31 | 1.07 |
SEM, standard error of the mean; L*, lightness; a*, redness; b*, yellowness.
Dietary treatments: Control, commercial broiler diet; CM, 17.5% CM inclusion; CMEnz, 17.5% CM inclusion+0.3 g/kg Axtra XAP; CMPh, 17.5% CM inclusion +1.5% Potassium Humate; CMEnzPh, 17.5% CM inclusion+1.5% PH+0.3 g/kg Axtra XAP.
Means in the same rows with different superscripts are significantly different (p<0.05).
Fatty acid profiles and nutritional indices of broiler meat
Diet had no effect (p>0.05) on the intramuscular fat (IMF) (Table 7). In the current study, the predominant fatty acids included the palmitic acid (C16:0), oleic acid (C18:1), linoleic acid (C18:2 n-6), and stearic acid (Table 8). Broilers fed on the control diet had higher values for most of the SFA, particularly myristic (C14:0) and palmitic (C16:0) acids. However, the canola fed broilers had higher values for most PUFAs including, the linoleic (C18:2 n-6), γLinolenic (C18:3 n-3), eicosadienoic, eicosatrienoic, decosapentaenoic, and decosahexaenoic acids. Interestingly, inclusion of humic acid in diets appeared to significantly increase the proportions of the n-3 PUFAs in broiler meat. The meat of broilers fed canola based diets were observed to be rich in PUFAs, total n-6 fatty acids and total n-3 fatty acids (Table 9). In the current study, inclusion of CM, humic acid and enzymes in diets resulted in an increase in PUFA/SFA ratio. Moreover, the inclusion of canola, humic acid and enzymes also reduced the n-6/n-3 ratio, particularly in the CMPh fed broilers although the values were above the recommended ratio of 5.
Table 7.
Parameter | Dietary treatments1) | SEM | ||||
---|---|---|---|---|---|---|
| ||||||
Control | CM | CMEnz | CMPh | CMEnzPh | ||
IMF | 1.67 | 1.73 | 1.50 | 1.31 | 1.54 | 0.16 |
FFDM | 22.99b | 22.87a | 22.11c | 24.18a | 22.58b | 0.27 |
Moisture | 75.34ab | 75.40ab | 76.38a | 74.51b | 75.87a | 0.24 |
SEM, standard error of the mean; IMF, intramuscular fat; FFDM, fat free dry matter.
Dietary treatments: Control, commercial broiler diet; CM, 17.5% CM inclusion; CMEnz, 17.5% CM inclusion+0.3 g/kg Axtra XAP; CMPh, 17.5% CM inclusion+1.5% Potassium Humate; CMEnzPh, 17.5% CM inclusion+1.5% PH+0.3 g/kg Axtra XAP.
Means in the same row with different superscripts are significantly different (p<0.05).
Table 8.
Fatty acids | Dietary treatments1) | SEM | ||||
---|---|---|---|---|---|---|
| ||||||
Control | CM | CMEnz | CMPh | CMEnzPh | ||
Myristic (C14:0) | 0.37a | 0.29b | 0.27c | 0.29b | 0.29b | 0.01 |
Myristoleic (C14:1c9) | 0.07a | 0.03b | 0.02b | 0.00b | 0.01b | 0.01 |
Pentadecylic (C15:0) | 0.08 | 0.08 | 0.07 | 0.09 | 0.08 | 0.01 |
Palmitic (C16:0) | 23.86a | 21.08c | 21.18bc | 22.07b | 21.86bc | 0.24 |
Palmitoleic (C16:1) | 4.65a | 2.58b | 2.35b | 1.80c | 2.46b | 0.24 |
Margaric (C17:0) | 0.94 | 0.96 | 1.05 | 1.29 | 0.93 | 0.09 |
Heptadecenoic (C17:1) | 0.06 | 0.14 | 0.19 | 0.09 | 0.14 | 0.07 |
Stearic acid (C18:0) | 8.01c | 8.09c | 9.07b | 9.84a | 8.39b | 0.42 |
Oleic (C18:1) | 30.43a | 26.72b | 26.28b | 25.36c | 26.67b | 0.77 |
Vaccenic (C18:1, 7) | 4.54a | 4.39b | 4.39b | 4.07c | 4.27b | 0.09 |
Nonoadecanoic (C19:0) | 0.47 | 0.48 | 0.53 | 0.66 | 0.46 | 0.05 |
Linoleic (C18:2, n-6) | 19.33c | 25.54a | 24.27a | 22.98b | 24.96a | 0.65 |
Arachidic (C20:0) | 0.04 | 0.05 | 0.04 | 0.04 | 0.03 | 0.01 |
α-Linolenic (C18:3 n-3) | 1.02d | 1.96a | 1.76b | 1.62c | 1.79b | 0.09 |
Heneicosanoic (C21:0) | 0.24 | 0.25 | 0.27 | 0.33 | 0.23 | 0.03 |
Eicosadienoic (C20:2, n-6) | 0.36c | 0.67a | 0.59b | 0.67a | 0.57b | 0.57 |
Eicosatrienoic (C20:3 n-6) | 0.03c | 0.10a | 0.09b | 0.11a | 0.07b | 0.01 |
Erucic (C22:1) | 0.83 | 0.76 | 0.75 | 0.84 | 0.70 | 0.07 |
Arachidonic (C20:4 n-6) | 3.72c | 4.39b | 5.25a | 5.94a | 4.69b | 0.49 |
Eicosopentaenoic C20:5 n-3) | 0.20 | 0.22 | 0.19 | 0.26 | 0.20 | 0.03 |
Docosapentaenoic (C22:5 n-3) | 0.32c | 0.63b | 0.69b | 0.81a | 0.62b | 0.06 |
Docosahexanoic (C22:6 n-3) | 0.18c | 0.38b | 0.46b | 0.61a | 0.37b | 0.06 |
SEM, standard error of the mean.
Dietary treatments: Control, commercial broiler diet; CM, 17.5% CM inclusion; CMEnz, 17.5% CM inclusion +0.3 g/kg Axtra XAP; CMPh, 17.5% CM inclusion+1.5% Potassium Humate; CMEnzPh, 17.5% CM inclusion+1.5% PH+0.3 g/kg Axtra XAP.
Means in the same row with different superscripts are significantly different (p<0.05).
Table 9.
Parameter | Dietary treatments1) | SEM | ||||
---|---|---|---|---|---|---|
| ||||||
Control | CM | CMEnz | CMPh | CMEnzPh | ||
Total SFA | 34.00a | 31.28c | 32.48b | 34.58a | 32.28b | 0.68 |
Total MUFA | 40.61a | 34.61b | 33.99bc | 32.17c | 34.25b | 4.25 |
Total PUFA | 25.39c | 34.09a | 33.53b | 33.25b | 33.47b | 0.62 |
Total n-6 | 23.52c | 30.68a | 30.23a | 29.73b | 30.33a | 0.58 |
Total n-3 | 1.88c | 3.42a | 3.29ab | 3.52a | 3.14b | 0.16 |
PUFA:SFA | 0.75c | 1.09a | 1.03a | 0.96b | 1.04a | 0.12 |
n-6/n-3 | 12.56a | 8.99bc | 9.22b | 8.47c | 9.68b | 0.21 |
SEM, standard error of the mean; SFA, total saturated fatty acids; MUFA, total mono unsaturated fatty acids; PUFA, total poly unsaturated fatty acids; n-6, total omega- 6 fatty acids; n-3, total omega-3 fatty acids.
Dietary treatments: Control, commercial broiler diet; CM, 17.5% CM inclusion; CMEnz, 17.5% CM inclusion +0.3 g/kg Axtra XAP; CMPh, 17.5% CM inclusion+1.5% Potassium Humate; CMEnzPh, 17.5% CM inclusion+1.5% PH+0.3 g/kg Axtra XAP.
Means in the same row with different superscripts are significantly different (p<0.05).
DISCUSSION
Carcass traits and internal organs
The higher breast weights of broilers fed humic acid and enzyme complex diets could be attributed to the effect of the humic acid and an enzyme complex in stimulating effective digestion and muscle accretion. According to Li et al [18] the inclusion of humic acid in broiler diets can improve digestion dynamics and nutrient absorption ultimately regulating growth and change the metabolism to enhance animal carcass traits. Moreover, Ozturk et al [10] and Kocabagli et al [19] also demonstrated a linear increase in body and carcass weights with the inclusion of humic acid substances in the broiler diet. On the other hand Dalólio et al [20], also reported a significant improvement on breast performance at 42 days for broilers supplemented with enzyme complex as observed in the current study. Diet, including other factors such as genetics, sex, slaughtering conditions and age of the animal can influence carcass traits [21,22]. Contrary to the current study Mateos et al [23] and Young et al [24] reported that broiler breast yield was reduced significantly when a diet of SBM was replaced with canola meal. Observation from the current study therefore confirm that inclusion of enzymes can improve utilisation of CM in broiler diets. The observed lack of differences in all other traits, apart from breast muscle weight and breast muscle ratio, in the current study is consistent with findings reported by Gopinger et al [25] where there was no effect of diet on carcass characteristics on broilers fed different protein sources at the growth and finisher phases.
Changes in size and structure of internal organs can be indicative of the effect of diet and its components on the development and function of the organs. The observed increase in weights of gizzards and spleen, and intestinal length could be attributed largely to the trophic effect of humic acid in stimulating the proliferation of normal cells and tissues, enhancing healthy tissue turnover and maintenance [18,26]. Moreover, the intestinal morphological alterations enhanced by humic acid could have the effect of increasing retention time of feed for digestion processes and enhancing mucosal permeability for efficient nutrient assimilation [26–28]. Findings from other studies, however, revealed lack of effect of diet on internal organs [29,30].
Meat quality
The visual appearance of meat is one of the most vital meat quality attributes that influence acceptance of meat and meat products and purchasing decisions by consumers [25,31]. The findings of the current study, showing lighter breast muscles in broilers fed the Control and CMPh diets are consistent with findings by Wang et al [12] and Adeyemi and Sazili [32] who observed that humic acid inclusion in diets can improve the appearance of the meat. Although the precise underlying mechanism of the effect of humic substances is unknown, it appears that humic substances contains minute quantities of several minerals, including Fe, Mn, and Cu, which may influence meat colour [33]. The observation that meat of broilers fed the control diet had the greatest WHC is in concordance with findings from other studies [34–36]. Although diet had no effect on both drip loss and cooking loss, it has been observed that, generally, greater drip loss may induce a reduction in water-holding capacity and tenderness of meat [12,37]. The WHC is generally associated with the lipid peroxides content in the muscle [38,39]. In the current study, the effect of diet on shear force values was insignificant. The shear force is an objective indicator of the toughness of the meat [40–42]. A lower shear force value is indicative of meat that is tenderer [25,42].
Fatty acid profiles and nutritional indices of broiler meat
Generally intra-muscular fat (IMF-marbling) content is an intrinsic indicator of meat quality [7,43]. The observed lack of influence of diet on IMF in the current study suggests that inclusion of CM, enzyme complex and humic acid salt in diets had no influence on fat biosynthesis during the regulation of IMF content [44]. Nevertheless the observed predominant fatty acids included the palmitic acid (C16:0), oleic acid (C18:1), linoleic acid (C18:2 n-6) and stearic acid are consistent with findings from other studies [3,45]. Broilers fed on the control diet had higher values for most of the SFA, particularly myristic (C14:0) and palmitic (C16:0) acids, which have a great significance due to their hypercholesterolemic properties that are related to coronary heart disease [3,46]. However, the canola fed broilers had higher values for most PUFAs including, the linoleic (C18:2 n-6), γLinolenic (C18:3 n-3), eicosadienoic, eicosatrienoic, decosapentaenoic, and decosahexaenoic acids which are essential for human health. Interestingly, inclusion of humic acid in diets appeared to significantly increase the proportions of the n-3 PUFAs in broiler meat. Although the underlying mechanism is still not well understood, in pork, humic acid was observed to increase fat marbling values and to reduce back fat thickness probably due its influence on protein and lipid digestibility and distribution that consequent in increased PUFA storage in the muscle tissue [12]. The increase in proportion of n-3 PUFAs in the CMPh fed broilers could also have been due to the influence of humic acid in increasing the efficiency of desaturase activities in the conversion of γLinolenic (ALA C18:3 n-3) to eicosapentaenoic acid (EPA 20:5n-3), docosapentaenoic (DPA 20:5 n-3), and docosahexaenoic acid (DHA 22:6n-3) [12].
The high PUFAs, total n-6 fatty acids and total n-3 fatty acids concentrations observed in broilers fed canola based diets could be a result of the contribution of protein source that was used in the diets in synergy with the activities of the feed additives in modulating the synthesis of intrinsic beneficial fatty acids that promotes the health of consumers. This is also supported by the higher values of PUFAs, total n-6 fatty acids and total n-3 fatty acids observed in the Canola-based diets (Table 3). According to FAO/WHO [47] and Grashorn [48], both n-3 and n-6 FAs in the meat play an immense role in human nutrition as they are originators of eicosanoids, leucotriens, and thromboxanes, which regulate the cardiovascular system and immunological processes [3]. The PUFA:SFA and n-6/n-3 ratios are critical parameters used to evaluate the nutritional value of meat [3,49]. Generally, meat with low PUFA:SFA ratio which is less than (0.4) and high n-6/n-3 ratio (>5) ratio may be considered to be poor and unfavourable since they might encourage an escalation in cholesterolaemia [49]. In the current study, inclusion of CM, humic acid and enzymes in diets resulted in an increase in PUFA/SFA ratio. Moreover, the inclusion of canola, humic acid and enzymes also reduced the n-6/n-3 ratio, particularly in the CMPh fed broilers although the values were above the recommended ratio of 5. Therefore, inclusion of canola, humic acid and enzymes resulted in a favourable effect on the level of important FAs required for maintenance of human health.
CONCLUSION AND APPLICATIONS
From the results, it can be concluded that the inclusion of enzymes (Axtra XAP) and potassium humate in canola-based broiler diets had beneficial effects on the carcass and meat quality parameters in terms of breast weights, WHC and colour coordinates. Inclusion of enzymes and potassium humate in canola-based broiler diets increased the proportion of PUFAs, n-6 and n-3 fatty acids and the PUFA/SFA ratio, which are important indicators of nutritional value of meat. Generally, inclusion of potassium humate in CM based diets alone resulted in greater benefits on intrinsic meat quality properties of broilers than that of the enzyme and the combination of the two in most instances did not yield any additional benefits.
ACKNOWLEDGMENTS
The authors thank the National Research Foundation, South Africa (NRF, SA) and the Health and Welfare Sector Education and Training Authority (HWSETA) for providing the research funds.
Footnotes
CONFLICT OF INTEREST
We certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript.
REFERENCES
- 1.Ozbey O, Esen F. The effects of breeding systems and stocking density on some blood parameters of rock partridges (Alectoris graeca) Poult Sci. 2007;86:420–2. doi: 10.1093/ps/86.2.420. [DOI] [PubMed] [Google Scholar]
- 2.Brenes A, Roura E. Essential oils in poultry nutrition: main effects and modes of action. Anim Feed Sci Technol. 2010;158:1–14. [Google Scholar]
- 3.Ahmed ST, Islam MM, Bostami ABMR, et al. Meat composition, fatty acid profile and oxidative stability of meat from broilers supplemented with pomegranate (Punica granatum L.) by-products. Food Chem. 2015;188:481–8. doi: 10.1016/j.foodchem.2015.04.140. [DOI] [PubMed] [Google Scholar]
- 4.Fang ZF, Peng J, Tang TJ, et al. Xylanase Supplementation improved digestibility and performance of growing pigs fed Chinese double-low rapeseed meal inclusion diets: in vitro and in vivo studies. Asian-Australas J Anim Sci. 2007;20:1721–8. [Google Scholar]
- 5.Wickramasuriya SS, Yi YJ, Kim JC, et al. A review of canola meal as an alternative feed ingredient for ducks. J Anim Sci Technol. 2015;57:29. doi: 10.1186/s40781-015-0062-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Cowieson AJ, Ravindran V. Effect of exogenous enzymes in maize-based diets varying in nutrient density for young broilers: growth performance and digestibility of energy, minerals and amino acids. Br Poult Sci. 2008;49:37–44. doi: 10.1080/00071660701812989. [DOI] [PubMed] [Google Scholar]
- 7.Yang Y, Song J, Fu R, Sun Y, Wen J. The expression of can and camk is associated with lipogenesis in the muscle of chicken. Brazilian J Poult Sci. 2009;9:287–92. [Google Scholar]
- 8.Yuan J, Yao J, Yang F, et al. Effects of supplementing different levels of a commercial enzyme complex on performance, nutrient availability, enzyme activity and gut morphology of broilers. Asian-Australas J Anim Sci. 2008;21:692–700. [Google Scholar]
- 9.Wiryawan KG, Dingle JG, Creswell D. Enzyme supplementation improves protein quality of grain legumes for poultry production. In: Corbett JL, Choct M, Rowe JB, Nolan JV, editors. Recent advances in animal nutrition in Australia. Armidale, Australia: University of New England; 1997. p. 231. [Google Scholar]
- 10.Ozturk E, Ocak N, Turan A, et al. Performance, carcass, gastrointestinal tract and meat quality traits, and selected blood parameters of broilers fed diets supplemented with humic substances. J Sci Food Agric. 2012;92:59–65. doi: 10.1002/jsfa.4541. [DOI] [PubMed] [Google Scholar]
- 11.Berg EP. Swine nutrition, the conversion of muscle to meat, and pork quality. In: Lewis AJ, Southern LL, editors. Swine nutrition. 2nd ed. Boca Raton, FL, USA: CRC Press; 2001. [Google Scholar]
- 12.Wang Q, Chen YJ, Yoo JS, et al. Effects of supplemental humic substances on growth performance, blood characteristics and meat quality in finishing pigs. Livest Sci. 2008;117:270–4. [Google Scholar]
- 13.Ragaa NM, Korany RMS. Studying the effect of formic acid and potassium diformate on performance, immunity and gut health of broiler chickens. Anim Nutr. 2016;2:296–302. doi: 10.1016/j.aninu.2016.08.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Folch J, Lees M, Sloane-Stanley H. A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem. 1957;226:497–509. [PubMed] [Google Scholar]
- 15.Aldai N, Nájera AI, Dugan MER, Celaya R, Osoro K. Characterization of intramuscular, intermuscular and subcutaneous adipose tissues in yearling bulls of different genetic groups. Meat Sci. 2007;76:682–91. doi: 10.1016/j.meatsci.2007.02.008. [DOI] [PubMed] [Google Scholar]
- 16.Alfaia CMM, Castro MFS, Martins IV, et al. Effect of slaughter season on fatty acid composition, conjugated linoleic acid isomers and nutritional value of intramuscular fat in Barrosã-PDO veal. Meat Sci. 2007;75:44–52. doi: 10.1016/j.meatsci.2006.06.013. [DOI] [PubMed] [Google Scholar]
- 17.SAS . Statistical Analysis System Institute Inc. Users guide. Carry, NC, USA: SAS Inc.; 2010. [Google Scholar]
- 18.Li XK, Wang JZ, Wang CQ, et al. Effect of dietary phosphorus levels on meat quality and lipid metabolism in broiler chickens. Food Chem. 2016;205:289–96. doi: 10.1016/j.foodchem.2016.02.133. [DOI] [PubMed] [Google Scholar]
- 19.Kocabagli N, Alp M, Acar N, Kahraman R. The effects of dietary humate supplementation on broiler growth and carcass yield. Poult Sci. 2002;81:227–30. doi: 10.1093/ps/81.2.227. [DOI] [PubMed] [Google Scholar]
- 20.Dalólio FS, Vaz DP, Moreira J, Albino LFT, Valadares LR. Carcass characteristics of broilers fed enzyme complex. Biotechnol Anim Husbandry. 2015;31:153–62. [Google Scholar]
- 21.Brickett KE, Dahiya JP, Classen HL, Gomis S. Influence of dietary nutrient density, feed form, and lighting on growth and meat yield of broiler chickens. Poult Sci. 2007;86:2172–81. doi: 10.1093/ps/86.10.2172. [DOI] [PubMed] [Google Scholar]
- 22.Havenstein GB, Ferket PR, Qureshi MA. Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult Sci. 2003;82:1509–18. doi: 10.1093/ps/82.10.1509. [DOI] [PubMed] [Google Scholar]
- 23.Mateos GG, Jiménez-Moreno E, Serrano MP, Lázaro RP. Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. J Appl Poult Res. 2012;21:156–74. [Google Scholar]
- 24.Young LL, Northcutt JK, Buhr RJ, Lyon CE, Ware GO. Effects of age, sex, and duration of postmortem aging on percentage yield of parts from broiler chicken carcasses. Poult Sci. 2001;80:376–9. doi: 10.1093/ps/80.3.376. [DOI] [PubMed] [Google Scholar]
- 25.Gopinger E, Xavier EG, Lemes JS, Moraes PO, Elias MO. Carcass yield and meat quality in broilers fed with canola meal. Br Poult Sci. 2014;55:817–23. doi: 10.1080/00071668.2014.980394. [DOI] [PubMed] [Google Scholar]
- 26.Ivarsson E, Wall H. Effects of toasting, inclusion levels and different enzyme supplementations of faba beans on growth performance of broiler chickens. J Appl Poult Res. 2017;26:467–75. [Google Scholar]
- 27.Disetlhe ARP, Marume U, Mlambo V, Dinev I. Humic acid and enzymes in canola-based broiler diets: Effects on bone development, intestinal histomorphology and immune development. S Afr J Anim Sci. 2017;47:6. [Google Scholar]
- 28.Nagaraju R, Reddy BSV, Gloridoss B, Suresh N, Ramesh C. Effect of dietary supplementation of humic acids on performance of broilers. Indian J Anim Sci. 2014;84:447–52. [Google Scholar]
- 29.Janječić Z, Grbeša D, Mužic S, et al. Influence of rapeseed meal on productivity and health of broiler chicks. Acta Vet Hung. 2002;50:37–50. doi: 10.1556/AVet.50.2002.1.6. [DOI] [PubMed] [Google Scholar]
- 30.Montazer-Sadegh R, Ebrahim-Nezhad Y, Maheri-Sis N. Replacement of different levels of rapeseed meal with soybean meal on broilers performance. Asian J Anim Vet. 2008;5:278–85. [Google Scholar]
- 31.Jiménez-Moreno E, González-Alvarado JM, González-Sánchez D, Lázaro R, Mateos GG. Effects of type and particle size of dietary fibre on growth performance and digestive traits of broilers from 1 to 21 days of age. Poult Sci. 2010;89:2197–212. doi: 10.3382/ps.2010-00771. [DOI] [PubMed] [Google Scholar]
- 32.Adeyemi KD, Sazili AQ. Efficacy of carcass electrical stimulation in meat quality enhancement: a review. Asian-Australas J Anim Sci. 2014;27:447–56. doi: 10.5713/ajas.2013.13463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Ji F, McGlone JJ, Kim SW. Effects of dietary humic substances on pig growth performance, carcass characteristics, and ammonia emission. J Anim Sci. 2006;84:2482–90. doi: 10.2527/jas.2005-206. [DOI] [PubMed] [Google Scholar]
- 34.Bai HX, Chang QF, Shi BM, Shan AS. Effects of fulvic acid on growth performance and meat quality in growing-finishing pigs. Livest Sci. 2013;158:118–23. [Google Scholar]
- 35.Ao T, Cantor AH, Pescatore AJ, Pierce JL. In vitro evaluation of feed grade enzymes activity at pH levels stimulating various parts of the avian digestive tract. Anim Feed Sci Technol. 2008;140:462–8. [Google Scholar]
- 36.Hughes JM, Oiseth SK, Purslowc PP, Warner RD. A structural approach to understanding the interactions between colour, water-holding capacity and tenderness. Meat Sci. 2014;98:520–32. doi: 10.1016/j.meatsci.2014.05.022. [DOI] [PubMed] [Google Scholar]
- 37.Pearce KL, Rosenvold K, Andersen HJ, Hopkins DL. Water distribution and mobility in meat during the conversion of muscle to meat and ageing and the impacts on fresh meat quality attributes. A review. Meat Sci. 2011;89:111–24. doi: 10.1016/j.meatsci.2011.04.007. [DOI] [PubMed] [Google Scholar]
- 38.Ari MM, Ayanwale BA, Ogah DM. Effects of alkali treatment of soybean on carcass traits, intestinal morphology and cooking yield of broilers. Trakia J Sci. 2013;2:189–96. [Google Scholar]
- 39.Macit M, Aksakal V, Emsen E, et al. Effects of vitamin E supplementation on performance and meat quality traits of Morkaraman male lambs. Meat Sci. 2003;63:51–5. doi: 10.1016/s0309-1740(02)00052-9. [DOI] [PubMed] [Google Scholar]
- 40.Schaefer DM, Liu Q, Faustman C, Yin MC. Supranutritional administration of vitamins E and C improves oxidative stability of beef. J Nutr. 1995;125:1792–8. doi: 10.1093/jn/125.suppl_6.1792S. [DOI] [PubMed] [Google Scholar]
- 41.Hofmann K. What is quality? Definition, measurement and evaluation of meat quality. Meat Focus Int. 1994;3:73–82. [Google Scholar]
- 42.Huff-Lonergan E, Baas TJ, Malek M, et al. Correlations among selected pork quality traits. J Anim Sci. 2002;80:617–27. doi: 10.2527/2002.803617x. [DOI] [PubMed] [Google Scholar]
- 43.Lonergan SM, Deeb N, Fedler CA, Lamont SL. Breast meat quality and composition in unique chicken populations. Poult Sci. 2003;82:1990–4. doi: 10.1093/ps/82.12.1990. [DOI] [PubMed] [Google Scholar]
- 44.Symeon S. Phospholipid metabolism and nuclear function: roles of the lipin family of phosphatidic acid phosphatases. Biochim Biophys Acta. 2013;1831:575–81. doi: 10.1016/j.bbalip.2012.09.014. [DOI] [PubMed] [Google Scholar]
- 45.Camerona ND, Enserb M, Nuteb GR, et al. Genotype with nutrition interaction on fatty acid composition of intramuscular fat and the relationship with flavour of pig meat. Meat Sci. 2000;55:187–95. doi: 10.1016/s0309-1740(99)00142-4. [DOI] [PubMed] [Google Scholar]
- 46.Laudadio V, Tufarelli V. Growth performance and carcass and meat quality of broiler chickens fed diets containing micronized-dehulled peas (Pisum sativum cv. Spirale) as a substitute of soybean meal. Poult Sci. 2010;89:1537–43. doi: 10.3382/ps.2010-00655. [DOI] [PubMed] [Google Scholar]
- 47.FAO/WHO Fats and fatty acids in human nutrition. Proceedings of the Joint FAO/WHO Expert Consultatio pern; November 10–14, 2008; Geneva, Switzerland. Ann Nutr Metab: 2009. pp. 5–300. [DOI] [PubMed] [Google Scholar]
- 48.Grashorn MA. Functionality of poultry meat. J Appl Poult Res. 2007;16:99–106. [Google Scholar]
- 49.Wang Q, Chen YJ, Yoo JS, et al. Effects of supplemental humic substances on growth performance, blood characteristics and meat quality in finishing pigs. Livest Sci. 2008;117:270–4. [Google Scholar]