The values of the feed consumption, egg weight, egg production and feed conversion ratio of the experimental groups are given in Table 2.
Table 2
The effect of propolis on the performance of laying hens consuming high-energy feed
Groups | Feed Consumption (g) | Egg Weight (g) | Egg Production (%) | Feed Convertion Ratio (g:g) |
Control | 115.01b | 61.58 | 79.97b | 2.35b |
HE + 0 mg/kg P | 110.26b | 61.46 | 71.51c | 2.62a |
HE + 100 mg/kg P | 127.16a | 61.67 | 87.19a | 2.38b |
HE + 200 mg/kg P | 128.88a | 63.29 | 86.33a | 2.39b |
HE + 300 mg/kg P | 109.44b | 60.53 | 68.57c | 2.77a |
SE | 2.61 | 0.35 | 1.95 | 0.06 |
P | * | ns | ** | * |
a-c: The averages shown with different letters in the same column are different from each other. HE: high energy, P: Propolis, Control: Basal fed group, HE + 0 mg/kg P: High energy fed group + 0 mg/kg propolis, HE + 100 mg/kg P: High energy fed + 100 mg/kg propolis, HE + 200 mg/kg P: High energy fed + 200 mg/kg propolis, HE + 300 mg/kg P: High energy fed + 300 mg/kg propolis, SE: Standard error, Ns:Not significant, *:P < 0.05, **:P < 0.01 |
No significant difference was found between the control group, the HE + 0 mg / kg propolis group and the 300 mg / kg propolis groups in terms of feed consumption. However, it was determined that adding 200 and 200 mg / kg propolis to feed increased feed intake significantly (P < 0.05). There was no significant difference between groups in terms of egg weight. It was determined that egg production was significantly lower in HE + 0 mg / kgP and HE + 300 mg / kg P groups compared to the control group, but the addition of 100 and 200 mg / kg propolis to a high-energy diet significantly increased egg production (P < 0.01). In the HE + 0 mg / kg P and HE + 300 mg / kg P groups, the degree of feed convertion ratio decreased significantly (P < 0.05).
It has been reported that propolis has antioxidative, anti-mutagenic and immunomodulatory properties and these properties are due to its rich flavonoid, phenolic acid and terpenoid content (Prytzyk et al., 2003; Wang et al., 2003.).The antioxidant properties of propolis are thought to be the cause of the increase in egg production and feed convertion ratio. In addition, the increase in feed consumption has been attributed to the aroma and anti-lipidemic effect of propolis. Similarly this study, Galal et al. (2008) reported that the addition of propolis to laying hen rations increased feed consumption, egg production, egg weight and improved feed efficiency. El-Neney and Awadien (2014) reported that layers fed diets supplemented with different levels of propolis (0.1, 0.2 or 0.3 g/kg) significantly improved feed efficiency per hen, egg production, egg weight and egg mass. It has been reported that the addition of 1 g/kg propolis in Japanese quails (Denli et al., 2005) and 2 g /kg propolis in ducks improved feed convertion ratio (Abdel-Rahman and Mosaad 2013). Abdel-Kareem and El-Sheikh (2017) found that adding different levels of propolis to laying hen feed did not affect feed intake but increased egg production and feed conversion ratio. Contrary to these studies, Belloni et al. (2015) reported that as the level of dietary propolis content (1.0–3.0%) in the layer's diet increased feed intake decreased. They suggested that this decrease in feed consumption may be due to the aroma of propolis.
Table 2
There was no significant difference between the groups in terms of values of egg quality criteria such as albumen ratio, yellow ratio, shell ratio, Hough Unit, shell breaking strength and shell thickness (Table 3).
Table 3
The effect of propolis on egg quality of laying hens consuming high-energy feed.
Groups | Albumen (%) | Yolk (%) | Egg shell (%) | Haugh Unit | Shell breaking strength (kg cm2) | Shell thickness (µm) |
Control | 61.25 | 28.66 | 10.09 | 80.21 | 2.40 | 0.449 |
HE + 0 mg/kg P | 57.45 | 31.91 | 10.63 | 83.55 | 2.11 | 0.472 |
HE + 100 mg/kg P | 56.57 | 32.23 | 11.19 | 83.58 | 3.21 | 0.481 |
HE + 200 mg/kg P | 58.16 | 31.37 | 10.46 | 85.75 | 3.15 | 0.431 |
HE + 300 mg/kg P | 58.45 | 29.97 | 11.61 | 81.03 | 2.91 | 0.482 |
SE | 0.60 | 0.50 | 0.20 | 0.90 | 0.26 | 0.008 |
P | ns | ns | ns | ns | ns | ns |
a-c: The averages shown with different letters in the same column are different from each other. HE: high energy, P: Propolis, Control: Basal fed group, HE + 0 mg/kg P: High energy fed group + 0 mg/kg propolis, HE + 100 mg/kg P: High energy fed + 100 mg/kg propolis, HE + 200 mg/kg P: High energy fed + 200 mg/kg propolis, HE + 300 mg/kg P: High energy fed + 300 mg/kg propolis, SE: Standard error, Ns:Not significant. |
Smilarly, it has been reported that the addition of propolis to laying hen rations does not affect the albumen, yolk and egg shell ratio, but increases the hough unit and shell thickness (Galal et al., 2008). Özkök et al. (2013) reported that propolis doses (0.1, 0.2 or 0.4 g/kg) had no dietary effect on quality criteria such as Haugh units and Shell thickness. However, Vilela et al. (2012) reported that propolis has a positive effect on the internal content of egg and quality of the egg shell. Abdel-Kareem and El-Sheikh (2017) reported that the addition of 1000 mg/kg propolis to laying hen diets increased weight of yolk and shell, Haugh unit and did not affect albumen weight.
Table 3
The means of wet weight, dry weight and fat ratio of liver are given in Table 4. The lowest values in terms of wet and dry liver weight were determined in the control and HE + 300 mg/kg P groups. The difference between the groups in terms of liver fat ratio was significant (P < 0.01), the highest value was found in the HE + 0 mg / kg P group, while the lowest value was observed in the HE + 300 mg / kg P group. Liver fat ratios of HE + 100 mg/kg P and HE + 200 mg/kg P groups were found to be considerably lower than the HE + 0 mg/kg P group.
Table 4
The effect of propolis on wet weight (g), dry weight (g) and fat ratio (%) of liver of laying hens consuming high-energy feed.
Groups | Wet weight of liver (g) | Dry weight og liver (g) | Fat ratio of liver % (DM) |
Control | 21.34b | 8.16b | 25.52c |
HE + 0 mg/kg P | 32.75a | 13.00a | 56.66a |
HE + 100 mg/kg P | 35.02a | 10.74a | 32.00b |
HE + 200 mg/kg P | 31.03a | 11.26a | 28.50b |
HE + 300 mg/kg P | 25.50b | 8.74b | 21.00d |
SE | 1.84 | 0.82 | 3.65 |
P | * | * | ** |
a-c: The averages shown with different letters in the same column are different from each other. HE: high energy, P: Propolis, Control: Basal fed group, HE + 0 mg/kg P: High energy fed group + 0 mg/kg propolis, HE + 100 mg/kg P: High energy fed + 100 mg/kg propolis, HE + 200 mg/kg P: High energy fed + 200 mg/kg propolis, HE + 300 mg/kg P: High energy fed + 300 mg/kg propolis, SE: Standard error, Ns:Not significant, *:P < 0.05, **:P < 0.01 |
It was determined that the addition of propolis to the diet increased the wet and dry weight of the liver in this study. Similarly, Hassan and Abdulla (2011) found that the addition of 400 mg/kg propolis to broiler diets increased liver weight.
It has been reported that the rate of liver fat exceeds 40% of the dry weight and can even reach 70% in the case of fatty liver (Ivy and Nesheim, 1973). In the present study, it was determined that the liver fat ratio (56.66%) was higher in the group fed with high energy feed (HE + 0% P) compared to the other groups. In many studies conducted in previous years, it was reported that the rate of liver fat increased in animals fed with high-energy feed (Splittgerber et al., 1969; Jensen et al., 1970; Akkılıç and Tanyolaç 1975). Rozenboim et al. (2016) reported that in laying hens fed a high-fat diet, the liver fat rate in young animals was not affected by diet, but the liver fat rate in old animals was lower than in the control group. Unlike mammals, fat synthesis is high in the liver of birds (Hermier, 1997). The liver plays a major role in fat synthesis and metabolism in laying hens. Similar to mammals, in avian species, the digestion and absorption of dietary fat occurs in the small intestine (Tancharoenrat et al. 2014). However, due to the poorly developed intestinal lymphatic system in birds, dietary fatty acids are discharged directly into the portal blood system (instead of the lymphatic system) in the form of very low density lipoproteins (VLDL) called portomicrons (Bensadoun and Rothfeld, 1972). Birds' liver becomes more prone to fat accumulation, as most portomicrons travel from the portal blood system to the liver before reaching the rest of the circulation (Cherian et al., 2002).
In the current study, it was determined that adding propolis to the high-energy diet significantly reduced the liver fat ratio compared to the control group. Lin et al. (1997) reported that 30 mg/kg propolis can prevent fatty liver degeneration caused by prolonged alcohol intake in human. Studies on the properties of propolis have shown that its addition to the diet protects liver tissue against the negative effects of various hepatotoxic factors (Banskota et al., 2000; Bazo et al., 2002; Bhadauria et al., 2009)
Table 4
There was no significant difference between the groups in terms of ALT, AST, glucose, total cholesterol and HDL cholesterol. The difference between the groups in terms of VLDL, TG and LDL cholesterol was significant (P < 0.01), with the highest values seen in the HE + 0 mg/ kg P group. It was observed that NEFA level increased significantly in the HE + 300 mg / kg propolis group.
In a study in which different levels of propolis were added to laying hen diets, it was reported that 1000 mg / kg propolis level increased toplam protein level, decreased ALT, AST and cholesterol levels (Abdel-Kareem and El-Sheikh, 2017). Galal et al. (2008) reported that blood triglyceride, cholesterol and ALT levels were significantly reduced in laying hens consuming 100–150 mg/kg propolis. In a study by Attia et al. (2014), it was reported that blood triglyceride and cholesterol concentrations were significantly reduced in chickens supplemented with 300 mg/kg propolis continuously for 35 days. The researchers argued that the decrease in these values was beneficial and safe by minimizing the liver function and reducing the harmful effects on the tissues of propolis treatment.
Koya-Miyata et al. (2009) found that propolis (5 mg/kg for 10 days) significantly reduced triglyceride, cholesterol, and NEFA levels in high fat diet mice. Hashem et al. (2013) reported in a study they conducted on rabbits that the addition of 150 mg/kg propolis reduced cholesterol, triglyceride levels, had no effect on LDL cholesterol, and increased HDL cholesterol. Kısmet et al. (2017) reported in their study on mice with non-alcoholic fatty liver that the addition of 100 and 200 mg of propolis to the ration reduced total cholesterol, triglyceride, HDL cholesterol, ALT and AST levels in serum.
Table 5
Table 5
The effect of propolis on some blood plasma biochemistry parameters of laying hens consuming high-energy feed.
| Control | HE + 0 mg/kg P | HE + 100 mg/kg P | HE + 200 mg/kg P | HE + 300 mg/kg P | SEM | P |
VLDL mg/dl | 96.00b | 304.50a | 157.33b | 65.66b | 113.66b | 26,36 | 0,020 |
ALT U/L | 3.00b | 7.00b | 3.00 | 3,66 | 3,66 | 0,66 | ns |
AST U/L | 256,6 | 314,50 | 218,33 | 313,33 | 265 | 18,92 | ns |
Glucose mg/dl | 257.00 | 245,50 | 259,33 | 288.00 | 277,66 | 6,64 | ns |
Total cholesterol mg/dl | 130,9 | 124.00 | 70,33 | 138.00 | 102.00 | 11,33 | ns |
TG mg/dl | 419.60b | 1323.00a | 785.00b | 328.66b | 568.00b | 131,87 | * |
HDL mg/dl | 43.00 | 35,5 | 27 | 49,66 | 30,66 | 4,96 | ns |
LDL mg/dl | 100.20b | 198.00a | 113.33b | 48.66b | 55.00b | 17,52 | ** |
NEFA (ng/L) | 0.219b | 0.220b | 0.221b | 0.211b | 0.505a | 0.035 | ** |
a-c: The averages shown with different letters in the same row in the are different from each other. HE: high energy, P: Propolis, Control: Basal fed group, HE + 0 mg/kg P: High energy fed group + 0 mg/kg propolis, HE + 100 mg/kg P: High energy fed + 100 mg/kg propolis, HE + 200 mg/kg P: High energy fed + 200 mg/kg propolis, HE + 300 mg/kg P: High energy fed + 300 mg/kg propolis, SE: Standard error, Ns:Not significant, *:P < 0.05, **:P < 0.01 |
There was a significant difference (P < 0.01) between the groups in terms of MDA, GSH, SOD, CAT and GPx values (Table 6). The highest Plasma MDA value and the lowest GSH, SOD, CAT and GPx values were detected in the HE + 300mg / kg P group.
Table 6
The effect of propolis on MDA and some enzyme activity of liver of laying hens consuming high-energy feed.
Groups | MDA (nmol/L) | GSH (nmol/L) | SOD (U/L) | CAT (KU/L) | GPx (U/L) |
Control | 7.64b | 2.30b | 58.16ab | 147.29b | 1.47b |
HE + 0 mg/kg P | 7.34b | 2.49a | 58.12ab | 152.63ab | 1.47b |
HE + 100mg/kg P | 7.84b | 2.15c | 55.94b | 152.83ab | 1.46b |
HE + 200mg/kg P | 7.55b | 2.57a | 60.12a | 162.97a | 1.57a |
HE + 300mg/kg P | 20.39a | 1.61d | 50.47c | 110.09c | 1.20c |
SEM | 1.55 | 0.10 | 1.08 | 5.86 | 0.038 |
P | ** | ** | ** | ** | ** |
a-d: The averages shown with different letters in the same column are different from each other. HE: high energy, P: Propolis, Control: Basal fed group, HE + 0 mg/kg P: High energy fed group + 0 mg/kg propolis, HE + 100 mg/kg P: High energy fed + 100 mg/kg propolis, HE + 200 mg/kg P: High energy fed + 200 mg/kg propolis, HE + 300 mg/kg P: High energy fed + 300 mg/kg propolis, SE: Standard error, Ns:Not significant, **:P < 0.01 |
Contrary to expectations, the MDA value in this study was determined to be the highest in the HE + 300 mg/kg P group, not in the HE + 0% P group. It was observed that MDA levels increased significantly in parallel with the NEFA value in the HE + 300 mg/kg propolis group (Table 5). In fatty liver symptom, overload of non esterated fatty acid (NEFA) level has been reported to trigger reactive oxidative stress formation through mitochondria-dependent oxidation or microsomal enzymes (Kısmet et al. 2017). Contrary to this study, Hashem et al. (2013) reported that the addition of 150 mg/kg propolis reduced MDA level in rabbits.
Catalase (CAT), glutathione peroxidase (GPX) and superoxide dismutase (SOD) are involved in the enzymatic antioxidant defense system of the body (Arya et al., 2021). While the highest SOD, CAT and GPx values were found in the 200 mg/kg Propolis group, the lowest values were found in the 300 mg/kg propolis group in this study. And the lowest GSH value was determined in the 300 mg/kg propolis group.
On the other hand, Arya et al. (2021) reported in a study they conducted on patients with nonalcoholic fatty liver syndrome that SOD and GPx levels were lower than the control group, and MDA value was higher. Similar to this study, it has been reported that there is a negative correlation between MDA and SOD in some other studies (Koruk et al. 2004: Videla et al.2004).
Table 6