https://orcid.org/0000-0002-8020-0971
Abstract
Chia (Salvia hispanica L.) is a member of Labiate family and its seeds are rich in phenolic compounds and polyunsaturated fatty acids (PUFAs) which could enhance the performance and productivity of birds. This study was carried out to determine the effects of supplementation with cold-pressed chia oil at different concentrations on the growth performance, carcase traits, haematology, blood chemistry, immunity and antioxidant status of growing quails. A total of 240 growing quails (1 week-old) were divided equally into five groups (4 replicates with 12 birds each). The experimental groups were G1 (basal diet), G2 (basal diet + 0.4 g chia oil/kg diet), G3 (basal diet + 0.8 g chia oil/kg diet), G4 (basal diet + 1.2 g chia oil/kg diet) and G5 (basal diet + 1.6 g chia oil/kg diet). Birds in the G2 group exhibited the highest body weight at 3 and 5 weeks of age, and the highest body weight gain at 1–3 weeks (6.24 g) and 1–5 weeks (6.17 g). Birds fed diets enriched with 0.4% chia oil exhibited the best FCR values. Dietary supplementation with chia oil increased the red blood cells (RBCs), white blood cells (WBCs), haemoglobin (HGB) and haematocrit (HCT) when compared to the control group (G1). The antioxidant and immunity parameters were not affected by the supplementation of diet with chia oil. This study showed that quail diet supplementation with 0.4 g chia oil/kg diet improved the growth performance, certain blood parameters and lipid profile.
Phytobiotics recently achieved an attention in poultry feed.
Cold-pressed chia oil dietary supplementation for quail diet.
G2 possessed the heaviest bodyweight and consumed the lowest feed with the best feed conversion ratio.
Quail diet supplementing with 0.4 chia oil/kg diet, improved the growth performance, some blood parameters, lipid profile and immunity.
Highlights
Introduction
Quail is a suitable bird for intensive food production, therefore, an attempt was made to enhance its production, and consequently guarantee adequate nutrition for the fast-growing human population. Consumption of two quails per day is akin to eating 125–130 g pure meat, which provides a total of 27–28 g protein, containing 11 g essential amino acids, equivalent to 40% of the human protein demand (Nedkov Citation2004). Currently, due to the global ban of antibiotic as growth promoters by the European Union, continuous attempts are conducted focussing on natural feed additives particularly herbal plants and their extracts as antibiotic replacers in animal and poultry feed owing to their content of natural bioactive compounds that can influence animal growth and health (Alagawany et al. Citation2019; Mohamed et al. Citation2019; Abd El-Hack et al. Citation2016, Citation2020; Reda, El-Kholy, et al. Citation2020; Reda, El-Saadony et al. 2020; Reda, Alagawany, et al. Citation2020). Chia seeds (Salvia hispanica L.) belong to the Lamiaceae family, and are believed to be a high-quality source of plant oils, which can be used as alternatives to other plant oils (Ayerza and Coates Citation2011). This may be attributed to their high omega-3 fatty acid contents. The oil content of these seeds is about 40% of their weight. Chia oil contains 60–70% omega-3 fatty acids, in particular α-linolenic acid (ALA or LNA), and 20% omega-6 fatty acids, particularly linoleic acid (Alagawany et al. Citation2019; Kulczy-ski et al. Citation2019; Mendonça et al. Citation2020). In addition, they contain several functional components, including myricetin, quercetin, kaempferol and caffeic acid, which are multifaceted phenolic acids and flavonols. These components have anticancer, antibacterial, anti-inflammatory and antioxidant effects (Uribe et al. Citation2011). Chia seeds are mainly composed of 15–25% protein, 30–33% fat, 41% carbohydrate, 18–30% dietary fibre, 4–5% ash and 90–93% dry matter, with a wide range of polyphenols (Ixtaina et al. Citation2008; Kulczy-ski et al. Citation2019).
The consumption of herbal plants or cold-pressed oils can enhance human and animal health and inhibit several diseases (Dhama et al. Citation2018; Mahgoub et al. Citation2019). The beneficial health aspects of chia seeds and oils on have been investigated in humans and animal, however, to our knowledge; studies on the supplementation of quail diets with chia oil are scarce. Therefore, this study was undertaken to investigate the effects of cold-pressed chia oil supplementation on the growth performance, carcase traits, haematology and blood chemistry and antioxidant and immunity status of growing quails.
Material and methods
Animals, experimental design, and diets
A total of 240 growing Japanese quails (1 week old), with an average weight of 30.07 ± 0.65 g, were randomly distributed into 5 experimental groups, each with 4 replicates and 12 birds/replicate. This 5-week study was conducted at the Poultry Research Farm, Department of Poultry, Faculty of Agriculture, Zagazig University, Zagazig, Egypt. The experimental groups were: (1) G1 (basal diet), (2) G2 (basal diet + 0.4 g chia oil/kg diet, (3) G3 (basal diet +0.8 g chia oil/kg diet, (4) G4 (basal diet + 1.2 g chia oil/kg diet) and (5) G5 (basal diet + 1.6 g chia oil/kg diet). The chia oil was obtained from the Elhawag Company for Natural OILS, Cairo, Egypt. The basal diet (Table ) was formulated to meet the birds’ requirements. Feed and water were provided ad libitum.
Table 1. Ingredients and nutrient contents of basal diet (as-fed basis) for growing Japanese quail.
Growth performance
Birds were weighed weekly to obtain the live body weight. Body gain for a given time interval was calculated by subtracting the average initial body weight of the birds from the final body weight during the same interval. The residual feed in the troughs was carefully collected and weighed. Feed consumption was calculated by subtracting the weekly residual feed from the offered feed. FCR was calculated weekly as the ratio of feed consumption (g) to body weight gain (g) (Reda, Alagawany, et al. Citation2020).
Carcase measurements
At the end of the experiment, five quails from each treatment group were selected, weighed and then slaughtered. The edible organs (carcase, gizzard, heart and liver) and intestine were removed and weighed. The carcase yield, or dressing percentage, was recorded. The whole organ weights were recorded in proportion to the pre-slaughter weight (Reda, Alagawany, et al. Citation2020).
Blood sampling and laboratory analyses
Blood samples from the slaughtered birds were collected into heparinised tubes, which were then closed with rubber stoppers. Haematological parameters (white blood cells [WBCs], lymphocytes [LYM], mid-range [MID], granulocytes [GRA], red blood cells [RBCs], haemoglobin [HGB], haematocrit [HCT], mean corpuscular volume [MCV], mean corpuscular HGB [MCH] and platelet count [PLT]) were determined according to Schalm (Citation1961). For assessing biochemical parameters, blood samples were centrifuged (G force rate = 2146.56×g) for 15 min. Plasma total protein (g/dL), globulin (g/dL), albumin (g/dL), aspartate transaminase (AST; IU/L), alanine transaminase (ALT; IU/L), creatinine (mg/dL), urea (mg/dL), total cholesterol (TC; mg/dL), triglyceride (TG; mg/dL), high-density lipoprotein (HDL) cholesterol (mg/dL) and low-density lipoprotein (LDL) cholesterol (mg/dL) levels were determined spectrophotometrically using commercial kits (Biodiagnostic Company, Giza, Egypt). The activities of superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px) and levels of malondialdehyde (MDA) and reduced glutathione (GSH) were determined in the plasma, using commercial kits and a spectrophotometer (Shimadzu, Japan). The immunoglobulin G (IgG; mg/dL) levels were measured using commercial kits. Complement C3 was determined in the plasma, using the ELISA Kit from MyBiosource.com (Catalogue number; MBS701356).
Statistical analysis
Data were analysed statistically using SAS. The growth rate, feed intake and conversion, carcase traits and haematological and biochemical (liver and kidney function, lipid profile, immunity and antioxidant indices) blood parameters were assessed by one-way ANOVA (with diet as the fixed factor) using the post-hoc Tukey’s test. The significance level was established at p<.05.
Results
Based on our results outlined in Table , it can be concluded that supplementation of quail diets with chia oil significantly improved the growth performance parameters. In comparison to the control group, supplementation with cold-pressed chia oil at levels of 0.4 and 0.8 g/kg diet resulted in higher (p < .0001) body weight at 3 weeks of age. However, at 5 weeks of age, all diets supplemented with chia oil, except G3, improved quail body weight (p i.0005). Birds in the G2 group exhibited the highest body weight at 3 and 5 weeks of age. The body weight of birds in this group was 12.96, 9.17, 11.54 and 13.81% higher at 3 weeks and 8.26, 5.97, 1.53 and 1.75% higher at 5 weeks, when compared to the weight of birds in G1, G3, G4 and G5 groups, respectively. Moreover, these birds presented the highest body weight gain at 1–3 weeks (6.24 g) and 1–5 weeks (6.17 g) when compared to the birds in the other groups (Table ). In comparison to the control, chia oil supplementation (G4 and G5) improved body weight gain at 3–5 and 1–5 weeks of age. Individuals in the G2 group not only exhibited the least feed consumption when compared to G1, G3, G4 and G5 at 1–3 weeks (24.41, 11.51, 0.56 and 10.46%, respectively) and 1–5 weeks (14.24, 6.82, 3.77 and 7.42%, respectively), but also presented the best FCR, which was higher by 50.50, 26.76, 18.68 and 35.35% than the other groups, respectively, at 1–3 weeks of age, and by 26.56, 14.76, 5.53 and 9.59%, respectively, at 1–5 weeks, respectively (Table ). However, no significant effects of chia oil could be observed on the carcase characteristics, including the dressing percentage and carcase, gizzard, liver, heart, intestine and giblet weights (p g.05; Table ).
Table 2. Effect of dietary supplementation on the growth performance of growing Japanese quail.
Table 3. Effect of dietary supplementation on carcase traits and relative organ weights of growing Japanese quail.
Dietary supplementation with chia oil resulted in higher RBCs, WBCs, HGB and HCT, when compared to the control group (G1), while LYM, MID, GRA, MCV, MCH and PLT did not exhibit any significant differences (Table ).
Table 4. Effect of dietary supplementation on haematological parameters of growing Japanese quail.
TP, GLOB, A/G, AST and creatinine did not show any significant differences between the experimental groups, while ALT was higher (p an.0109) in groups fed diet supplemented with chia oil at different concentrations, when compared to the control group (G1). Urea level was lower in G2 than in G3 and G4 (38.26 and 68.69%, respectively) (p 38.0004; Table ). TC was reduced by supplementation with chia oil, with LDL being the lowest in G2 and G5 (Table ). The antioxidant and immunity parameters were not influenced by dietary supplementation with chia oil at any of the tested concentrations (p > .05; Table ).
Table 5. Effect of dietary supplementation on liver and kidney functions of growing Japanese quail.
Table 6. Effect of dietary supplementation on the lipid profile of growing Japanese quail.
Table 7. Effect of dietary supplementation on the antioxidant and immunological indices of growing Japanese quail.
Discussion
The FCR is the imperative economic aspect which describes the effectiveness of feed consumption and its conversion into production unit. It combines two chief traits, i.e. weight gain and feed consumption. The results on body weight obtained in this study were comparable to those reported by Nasr et al. (Citation2017), who stated that quail body weight at 6 weeks of age ranges from 175 to 205 g. Moreover, the FCR of the group fed the normal basal diet was within the normal reported range of 2.87–3.93 g feed/g gain (Rasul et al. Citation2019; Nasr et al. Citation2019). Chia oil supplementation not only improved the FCR, confirming the results of Rasul et al. (Citation2019), who reported that chia seed supplementation improved the FCR by 4.74%, but also reduced the feed consumption, which was comparable to the findings of Abbasi and Samadi (Citation2014) and Mendonça et al. (Citation2020) who observed a reduction in feed intake (4% and 9.31) on chia supplementation, respectively. The feed intake in this study was similar to that reported in Abdelhady et al. (Citation2018). On the same context, broiler diet containing 2.5% chia oil improved the FCR by 6.80% during the period from 29 to 42 d of age (Mendonça et al. Citation2020).
In this study, chia oil supplementation reduced feed intake, improved body weight, body weight gain, and FCR, supporting the previous findings of Asad et al. (Citation2019) and Rasul et al. (Citation2019), who reported that chia seed increased the body weight and improved the FCR in broilers. This improvement may be due to several factors, such as; a) presence of a sufficient quantity of polyphenolic compounds in chia (caffeic acid, chlorogenic acid, kaemperol, myricetin and quercetin) which are potent antioxidants that can reduce the production of free radicals in the body, inhibit peroxidation of fats and have much stronger antioxidant activities than vitamin C, vitamin E and ferulic acid, b) presence of large amounts of vitamins (A, C and E) and minerals (sodium, potassium and chloride) in chia oil that might play a role in stress reduction, c) increased digestive secretion (bile and mucus) and stimulation of enzymatic activities, d) improved digestive tract motility, food taste, and immunity and antimicrobial status, e) increased trypsin, amylase and jejunal chyme secretion, f) diminished bacterial adherence (i.e. Escherichia coli and Clostridium perfringens) to the intestinal wall (Pandey and Rizvi Citation2009; Nadeem et al. Citation2014; Alagawany et al. Citation2018, Citation2019; Kulczy-ski et al. Citation2019; Mendonça et al. Citation2020).
In contrast, Ayerza et al. (Citation2002) reported that chia seed supplementation resulted in lower feed conversion and reduced body weight. They attributed this to the presence of the polysaccharide mucilaginous gel, which firmly coats the seeds. The gum may pose a physical barrier to fat extraction from the seed, resulting in inferior metabolisable energy in broilers fed with chia seeds. Moreover, visual detection of whole chia seeds in the excreta of birds fed with chia confirmed these findings, and the authors suggested that supplementation with ground chia or chia oil may reduce this effect. However, this was not the case in our experiment.
Dressing percentage is a superior index of whole edible meat after the removal of viscera, blood and feathers (Mohamed et al. Citation2019). There are conflicting results regarding the effects of dietary phytogenic supplementation on carcase traits. Kana et al. (Citation2017) found no difference in carcase traits, while Simsek et al. (Citation2007) reported a significant effect on carcase yield and traits. Our results were consistent with those of the majority of investigations that did not find any significant effect of phytogenic oil supplementation on carcase traits (Reda, Alagawany, et al. Citation2020). The percentage carcase yield of the different experimental groups in this study was within the range reported by Abdelhady et al. (Citation2018) for quails, i.e. 67–88.1%. However, it was lower than that reported by Nasr et al. (Citation2017). Furthermore, Rasul et al. (Citation2019) reported that chia supplementation had no significant impact on the dressing percentage (56.94% in basal diet vs. 57.86% in chia supplemented diet). The carcase yield percentage of Japanese quail is affected by slaughter age, breed, line and sex of quails (Abou-Kassem et al. Citation2019; Mohamed et al. Citation2019; Reda, Alagawany, et al. Citation2020). Our results regarding the percentage liver weight were almost similar to the findings (2.35–2.48%) of Rasul et al. (Citation2019); however, the percentage gizzard and heart weights were found to be higher in this study, whereas the percentage giblet weight was comparable to the range (4.63–7.52%) reported by Abdelhady et al. (Citation2018).
Haematology is a critical marker of physiological or pathophysiological conditions of the animal body (Farag et al. Citation2019). The HCT level represents the percentage of blood which is composed of RBCs after centrifugation. HCT is affected by RBC number and size. Moreover, it is a marker of the total number of RBCs, which determines the oxygen-carrying capacity (Maheswaran et al. Citation2008). The haematological parameters observed in this study were within the normal ranges reported for quails, i.e. 1.06–4.34 × 106 RBC/μL (Pravda et al. Citation1996), 7.57–15 g/dL HGB (Mnisi et al. Citation2017), 88.24–433.96 µm3 MCV (Pravda et al. Citation1996) and 25.27–104.62 pg MCH (Pravda et al. Citation1996).
In this study, chia oil supplementation improved the WBCs, RBCs, HGB and HCT%. These results may be attributed to the anabolic hormones (thyroid hormones), which are responsible for increasing the RBCs. Increasing WBCs is favourable as leukocytes provide quick and robust protection against substances that may trigger infection. Several factors affect leukocyte values in poultry, such as the genetic makeup, stress condition, rearing system, diet, production stage and lighting period (Hrabcakova et al. Citation2014). These factors may explain the contradiction between the results of this study and those of Toghyani et al. (Citation2010), who did not observe any significant effect of phytogenic supplements (thyme powder) on broiler WBCs, RBCs, HGB and HCT%.
Liver is the site of protein synthesis and its cells normally contain AST and ALT. Disturbance of protein level and the leakage of ALT or AST into blood occurs in certain conditions, such as hepatitis, congestive heart failure, liver or bile damage and cellular necrosis; therefore, measuring serum levels of ALT, AST, total protein, albumin and globulin are important in determining liver performance (Evans Citation2009). In this study, chia oil did not alter liver function and did not exert any negative impact on liver weight, suggesting that chia does not contain high amounts of anti-nutritional compounds, which necessitate detoxification. The urea levels were higher in birds in G3, G4 and G5 groups than in the group fed the basal diet. The observed urea level was within the range (1.14–3.05 mmol/L) reported by Mnisi et al. (Citation2017). This is further supported by the findings of Ngouana Tadjong et al. (Citation2017), who observed that supplementation of broiler diet with essential oils encapsulated in chitosan and charcoal elevated the serum urea levels of. However, chia oil supplementation at 0.4 g/kg diet reduced the serum urea level, which is consistent with Ahmed (Citation2019), who found that supplementation of quail feed with chia seeds lowered the uric acid levels. The author further stated that adding chia seeds to quail diet did not affect the globulin levels and albumin/globulin ratio, which is consistent with our results. Moreover, creatinine, which is a dependable marker of kidney function, was not affected by chia oil supplementation. This result was consistent with that of Evans (Citation2009), and the observed level was similar to Mnisi et al. (Citation2017), who reported a normal creatinine level of 0.35 mg/dL for quail blood. These observations could be returned to absence of the toxic substances in chia seeds or oils which are present in other plant seeds or fish meals (Ting et al. Citation1990; Ayerza and Coates Citation1999; Mendonça et al. Citation2020).
Chia oil supplementation in this study resulted in lower serum TC levels when compared to the control group, which was consistent with several previous studies (Ahmed Citation2019; Asad et al. Citation2019; Rasul et al. Citation2019) which also showed that such a dietary supplementation also alleviated stress and improved the immune status. Moreover, chia seeds also decreased the level of cholesterol in pig meat and chicken meat and eggs (Ayerza et al. Citation2002; Antruejo et al. Citation2011). In addition, the observed TC values were within the range reported (86–276 /dL) by Rasul et al. (Citation2019). This effect can be attributed to the enhancement of omega-3 unsaturated fatty acid (Ayerza et al. Citation2002) and omega-6 fatty acid (Antruejo et al. Citation2011) levels by chia seeds. These fatty acids prevent cholesterol synthesis in several ways: a) by lowering its re-absorption through the small intestine, b) by impeding the activity of 7 alpha-hydroxylase and beta-hydroxy methylglutaryl-CoA enzymes that transfer cholesterol to bile acids and c) by restricting the build-up of cholesterol by converting mevalonate to squalene (Kheiri et al. Citation2015). Furthermore, the presence of natural antioxidants in chia oil plays a role in the reduction of cholesterol levels (Ahmed Citation2019).
Previous studies have yielded inconsistent results on the effect of dietary chia supplementation on plasma triglyceride levels, i.e. Rahimi et al. (Citation2011) reported a reduction, whereas Ahmed (Citation2019) found an elevation in their levels. We found a reduction in the serum triglyceride levels of birds supplemented with chia oil, especially in the G2 group, which is consistent with some previous works. This reduction may be attributed to the presence of omega-3 and omega-6 fatty acids (Antruejo et al. Citation2011; Rahimi et al. Citation2011; Alagawany et al. Citation2019) and the activity of natural antioxidants in chia (Ahmed Citation2019).
Chia oil supplementation decreased the LDL levels, which is in agreement with the results obtained by supplementation of chia seeds (Ahmed Citation2019). This reduction confirmed the lower cholesterol levels observed in this study because HDL and LDL molecules are the chief transporters of cholesterol from its site of synthesis, i.e. the liver, to the body tissues and they consequently decrease cholesterol and triglycerides available for tissue metabolism, lipogenesis in liver and fat accumulation in carcases (Alvarenga et al. Citation2011). In the present investigation, LDL levels in the groups supplemented with chia oil (especially G2) were similar to those reported by Abdelhady et al. (Citation2018).
The antioxidant systems in the body consist of antioxidant enzymes, i.e. SOD and GSH-Px that protect the body from oxidative stress. The concentrations of MDA and GSH are used as indicators for evaluating antioxidant systems. Total antioxidant capacity is commonly used to evaluate the antioxidant condition of biological samples and to detect the antioxidant response to free radicals released under stress conditions. The quantity of free radicals in the body increases during stress, and chia seeds can deactivate these radicals and defend the body during stress (Nadeem et al. Citation2014). Recent studies have shown that phenolic compounds have positive effects on the body because of their antioxidant, anti-inflammatory and antimicrobial properties. Akbarian et al. (Citation2015) found that dietary supplementation with plant extracts rich in phenolic compounds in chickens exposed to chronic thermal stress resulted in an elevation of their blood GSH-Px activity. Several investigations have shown that chia seeds can be used as anti-stressors, as they are a good source of antioxidants, which can be used for health improvement (Uribe et al. Citation2011). Our results showed that there was no significant difference between groups supplemented with different levels of chia oil and the group fed the basal diet, which indicates that the feed used in this study was a good source of antioxidants.
Complement 3 plays a role in innate immunity (the chief component of the immune system) by attaching to the cell membranes of pathogenic microbes and enhancing the effectiveness of phagocytic cells and antibodies to get rid of microbes and injured cells from the body (Ricklin et al. Citation2016). Dietary supplementation with antioxidants may upgrade broiler performance and immunity by reducing the thiobarbituric acid values in the liver and increasing serum and liver vitamin A and E levels (Tavárez et al. Citation2011). Moreover, broiler diet supplementation with plant products with high antioxidant compound contents can improve the oxygen scavenging responses to preserve fat sources both outside and inside the body (Ahmed Citation2019). Supplementing the diet with chia (0.4 g/kg diet) improved the immune status of quails, confirming the results recently reported by Asad et al. (Citation2019), who observed an enhancement of the immune response of broilers fed a diet supplemented with chia seeds. These outcomes may be related to the presence of antioxidants in chia that can aid in improving health (Uribe et al. Citation2011), and it is also considered a good source of omega-3 fatty acids (n-3 polyunsaturated fatty acid (PUFA) and ALA). The n-3 PUFAs are more efficient than ALA in boosting the immune responses (Alagawany et al. Citation2019). Moreover, the protein content of chia has been proved to enhance the development of thymus gland and consequently the immune status (Fernandez et al. Citation2008). Ayerza and Coates (Citation2005) also reported that all forms of chia did not induce abnormal behaviour, inflammations, digestive disturbances or other signs of diseases. On the other hand, chia oil reduced the Σω-6:Σω-3 ratio and the thrombogenicity and atherogenicity indices of the broiler chicken meat, providing improvements in the meat nutritional quality, with consequent health benefits for its consumers (Mendonça et al. Citation2020).
Conclusions
This study showed that supplementation of quail diet with 0.4 g chia oil/kg diet improved the growth performance, some blood parameters, lipid profile and immunity, supporting the idea that phytogenics may possess complicated mechanisms of action, which can alter feed colour and flavour, enhance gastric motility and upgrade the secretion of digestive enzymes, antioxidant levels and endocrine and immune functions.
Ethical approval
Animal care and maintenance were performed in accordance with the guidelines of the Egyptian Research Ethics Committee and the guidelines specified in the Guide for the Care and Use of Laboratory Animals (2011).
Acknowledgements
The authors extend their acknowledgement to the Deanship of Scientific Research at King Saud University for funding this work through research group No (RG-1440-146). The authors thank the Deanship of Scientific Research and RSSU at King Saud University for their technical support.
Disclosure statement
No potential conflicts of interest declared.
Additional information
Funding
References
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