Citation of this paper

Effect of dietary lycopene supplementation on growth performance, blood parameters and antioxidant enzymes status in broiler chickens

Aref Mezbani, Bahman Parizadian Kavan, Ali Kiani and Babak Masouri

Department of Animal Science, Lorestan University, Khorramabad, Iran
bahman.kavan@gmail.com

Abstract

This study was conducted to evaluate the effects of dietary supplementation with lycopene on growth performance, blood parameters and antioxidant enzymes in broiler chickens. A total of 240 male broiler chickens (Ross 308 strain) were used in a completely randomized design with four treatments with five replicates and 12 chicks per each. The broilers were fed a standard grower diet supplemented with lycopene (0, 50, 100 and 200 mg/kg) from 21 to 42 days. Results showed that adding of lycopene (100 mg/kg) in broiler's diet increased body weight gain. Supplementing with lycopene (200 mg/kg) resulted in significant increases in the feed intake. Broilers that were fed with lycopene (100 mg/kg) had the lower feed conversion ratio compared with control group. Supplementation of lycopene (100 mg/kg) significantly decreased the serum concentrations of cholesterol, triglyceride and VLDL. HDL content in serum was increased by the inclusion of lycopene (100 mg/kg). Serum malondialdehyde level was decreased in lycopene supplemented groups (100 mg/kg) compared to control group. The highest content of catalase and glutathione peroxidase in serum were observed in group supplemented with 100 mg of lycopene. Dietary lycopene (100 mg/kg), as compared with the control diet, decreased serum activity of alkaline phosphatase and alanine aminotransferase. In conclusion, diet supplementation with lycopene improved performance and antioxidant status of broilers.

Keywords: carotenoid, liver, malondialdehyde, tomato

Introduction

In broiler, oxidative stress caused by reactive oxygen species (ROS) constitutes an important mechanism that may lead to biological damages, serious health disorders, and impaired growth rates (Fellenberg and Speisky 2006). Nutrition plays an important role in maintaining the pro-oxidant-antioxidant balance (Cowey 1986). The use of antioxidant compounds in feeding of broilers can improve immune function and reduce deleterious effects of ROS on cells (Tawfeek et al 2014). Carotenoids in general considered as antioxidants (Chew 1993; Milani et al 2017). Lycopene (C₄₀H₅₆) is a member of the carotenoid family with no pro-vitamin A activity (Rao and Rao 2007) and functions as a very potent antioxidant (Heber and Lu 2002). Lycopene is a natural pigment soluble in lipid and found in many red color fruits and vegetables such as tomatoes (Shi 2000). Lycopene acts as a powerful antioxidant and free radical quencher due to its multiple conjugated double bonds. The antioxidant activity (singlet oxygen activity and peroxyl radical scavenging) of lycopene is twice as powerful as that of beta-carotene and 10 times higher that of alpha-tocopherol in quenching ability (Agarwal and Rao 2000). Lycopene inhibits lymphocyte proliferation through mechanisms dependent on early cell activation (Mills et al 2012). It has been shown that lycopene supplementation could improve antioxidant capacity and immune function, and regulate lipid metabolism in chicks (Lee et al 2016; Sun et al 2015). Lycopene reduces the negative effects induced by lipopolysaccharide in breeding hens (Sun et al 2014a). In another study conducted with Englmaierova et al (2011), it was reported that a diet supplemented with lycopene decreased cholesterol content in the meat of broilers. Sun et al (2014b) have shown that serum lipid profile improved by dietary lycopene supplementation in breeding hens. Recently, Sahin et al (2016) reported that, lycopene activated antioxidant enzymes and nuclear transcription factor systems in heat-stressed broilers. We hypothesis that lycopene alleviate oxidative stress by affecting oxidative enzymes and lipid metabolism, hence improving the growth performance of growing broilers. Therefore, in the present study the effect of different level of lycopene on antioxidant enzyme activity, blood lipid profile and growth rate in broiler chicks was investigated.

Materials and methods

Birds and experimental design

In this experiment 240 broiler chicks (Ross 308) from 21 to 42 days of age in four treatments and five pens (12 birds per replicate) were used in a completely randomized design. The birds were randomly assigned to four groups. Chicks were fed with a standard basal diet (control) or basal diet supplemented with 50, 100 and 200 mg/kg lycopene. The birds were reared from 21 to 42 days. The chickens were housed in cages (100×110 cm). Each cage was equipped with bell-drinker and a feeder. The broiler chickens were fed a basal diet formulated to meet minimum nutrient requirements (NRC 1994). The diets were formulated using UFFDA software. The composition and the calculated nutrient content of the experimental diets are presented in Table 1. Experimental diets (in mash form) and water were provided ad libitum. A continuous lighting program was provided during the experiment (23 h L:1 h D).

Table 1. Ingredient and nutrient composition of the diet
Ingredient (%)	Starter diet (1-21 d)	Grower diet (22-42 d)

Corn	52.8	61.6
Soybean meal	40.0	32.0
Soybean oil	3.4	3.1
Dicalcium phosphate	1.7	1.4
Limestone	1.3	1.1
Salt	0.3	0.3
Vitamin premix	0.2	0.2
Mineral premix	0.2	0.2
DL-Methionine	0.1	0.1
*Calculated composition*
ME, kcal/kg	2966.1	3050.5
Crude protein, %	21.8	19.0
Lysine, %	1.1	0.9
Methionine+ cystine, %	0.7	0.6
Calcium, %	0.9	0.8
Available phosphorus, %	0.4	0.4
Each kg of vitamin premix contained: Vitamin A, 3,500,000 IU; Vitamin D₃, 1,000,000 IU; Vitamin E, 9000 IU; Vitamin K₃, 1000 mg; Vitamin B₁, 900 mg; Vitamin B₂, 3,300 mg; Vitamin B₃, 5,000 mg; Vitamin B ₅, 15,000 mg; Vitamin B₆, 150 mg; Vitamin B₉, 500 mg; Vitamin B₁₂, 7.5 mg; Biotin, 500 mg; Choline chloride, 250,000 mg. Each kg of mineral premix contained: Mn, 50,000 mg; Fe, 25,000 mg; Zn, 50,000 mg; Cu, 5,000 mg; I, 500 mg; Se, 100 mg.

Growth performance measurements

Performance data were recorded in the periods from 21 to 28, 29 to 35, 36 to 42 and 21 to 42 days of age. Feed intake (FI) was determined for each repetition as the difference between the amount of feed supplied and the remained feed at the end of each experimental period, and body weight gain (BWG) was calculated as the difference between the final and initial bird weight. Feed conversion ratio (FCR) was determined as the ratio between feed intake and weight gain at each phase of the experimental period.

Carcass Traits

On d 42, two chicks whose body weights were similar to the group average were selected from each pen and slaughtered by severing the carotid artery and jugular veins. Carcass weight measurements were done after defeathering. Heads, necks, and feet were removed from the birds, and then carcasses were eviscerated and weighted to determine the percentage of carcass yield. Measurements included hot carcass yield, carcass components (weight of eviscerated carcass and some internal organs), and abdominal fat content. The weights of breast, thigh, liver, heart, pancreas and abdominal fat were individually measured. The weights of internal organs were expressed as a percentage of live body weight. The hot carcass yield was calculated as a percentage of preslaughter body weight.

Serum Biochemical Parameters

On day 21 of experiment, 5 ml of blood was collected from wing vein from 10 birds in each treatment, blood samples were centrifuged (2,000× g for 10 min) and serum was separated and then stored at -20^oC until assayed for measuring biochemical parameters such as glucose, cholesterol, triglyceride, high-density lipoprotein (HDL), low-density lipoprotein (LDL), very low density lipoprotein (VLDL), aspartate amino transferase (AST), alanine amino transferase (ALT) and alkaline phosphatase (ALP) using appropriate laboratory kits (Pars Azmoon, Tehran, Iran) (Gowenlock et al 1988).

Antioxidant Capacity

Catalase (CAT) activity was measured by the rate of H₂O₂ disappearance according to Aebi (1974). Glutathione peroxidase (GSH-Px) activity was determined using the procedure of Beutler (1957). Malondialdehyde (MDA) levels in serum was determined using the thiobarbituric acid distillation method described by Tarladgis et al (1960).

Statistical Analysis

The data obtained from the experiment were analyzed by using SAS (SAS Institute 1999) statistical programs with the ANOVA. Significant differences among treatment means were separated using Duncan^, s multiple range test with a 5% probability (Duncan 1955).

Results and discussion

BWG increased significantly for broilers fed diet supplemented with lycopene (100 mg/kg) compared with the control treatment throughout the experimental period (Table 2). The highest FI was for broilers treated with lycopene throughout the experimental period. Supplementation of lycopene (100 mg/kg) in the diets improved the FCR throughout the experimental period. The addition of lycopene to the diet had no significant impact on carcass traits of broilers in this study (Table 3).

Dietary lycopene supplementation (100 mg/kg) caused significant increases in serum glucose level compared with the control group (Table 4). Supplementation of lycopene (100 mg/kg) significantly decreased the serum concentrations of cholesterol, triglyceride and VLDL. HDL content in serum was increased by the inclusion of lycopene (100 mg/kg) (p< 0.05). No significant difference was found in serum LDL level among different treatments.

Dietary inclusion of lycopene (100 mg/kg) caused a significant decrease in serum MDA concentration (Table 5). In contrast with the control group, supplementation of diets with lycopene (100 mg/kg) elevated CAT and GSH-Px activities in serum.

The AST was not influenced by lycopene (Table 6). The addition of lycopene (100 mg/kg) as a supplement to broilers diets reduced the ALT and ALP concentration.

Table 2. Effects of dietary lycopene level on performance of broilers
Parameters	Lycopene supplementation (mg/ kg)				SEM	p
BWG (g)	Control	50	100	200	SEM	p

21-28 d	59.2	61.2	62.1	56.1	2.0	0.2
29-35 d	65.6^c	73.6^bc	79.4^a	76.2^b	1.2	<0.001
36-42 d	50.5^c	75.8^b	77.8^ab	79.0^a	1.7	<0.001
21-42 d	58.4^b	70.2^ab	73.1^a	70.5^ab	1.0	<0.001
*FI (g)*
21-28 d	103^a	92.4^b	89.6^bc	85.3^c	1.6	<0.001
29-35 d	106^b	122^ab	125^a	126^a	2.4	0.0003
36-42 d	100^b	128^ab	128^ab	133^a	2.1	<0.001
21-42 d	103^b	114^a	114^a	114^a	1.1	<0.001
*FCR (g:g)*
21-28 d	1.7^b	1.5^a	1.4^a	1.5^a	0.05	0.03
29-35 d	1.6	1.6	1.5	1.6	0.04	0.6
36-42 d	1.9^b	1.7^a	1.6^a	1.6^a	0.05	0.009
21-42 d	1.7^b	1.6^a	1.5^a	1.6^a	0.02	0.006
^{a, b, c} Mean values in the same row with different superscript letters were significantly different (p<0.05). BWG, body weight gain; FI, feed intake; FCR, feed conversion ratio .

Table 3. Effects of dietary lycopene level (mg/ kg) on carcass traits (%) of broilers
Treatments	Carcase yield	Breast	Thigh	Liver	Pancreas	Heart	Abdominal fat

Control	64.0	24.9	19.8	1.7	0.2	0.5	0.9
50	65.7	24.9	19.9	1.9	0.2	0.4	0.8
100	67.1	24.9	19.9	1.9	0.2	0.4	0.7
200	65.9	24.8	19.8	1.8	0.2	0.4	0.8
SEM	1.6	0.5	0.4	0.5	0.008	0.02	0.03
P-value	0.6	0.9	0.9	0.7	0.1	0.07	0.1

Table 4. Effects of supplemental lycopene (mg/ kg) on serum biochemical parameters (mg/dL) of broilers
Treatments	Glucose	Cholesterol	Triglyceride	HDL	LDL	VLDL

Control	202^c	151^a	63.7^a	25.9^b	112	12.7^a
50	208^bc	135^b	51.0^b	30.2^b	95.0	10.2^b
100	219^a	121^c	46.7^b	42.7^a	68.9	9.3^b
200	215^ab	126^bc	50.5^b	38.6^a	77.8	10.1^b
SEM	2.8	2.6	1.7	1.7	12.4	0.3
P-value	0.01	<0.001	0.002	0.0001	0.1	0.002
^{a, b, c} Mean values in the same column with different superscript letters were significantly different (p<0.05) HDL, high-density lipoprotein; LDL, low-density lipoprotein; VLDL, very low density lipoprotein.

Table 5. Effects of dietary lycopene level (mg/ kg) on antioxidant status in broilers
Treatments	CAT (U/mg of protein)	GSH-Px (U/mg of protein)	MDA (μmol/mg of protein)

Control	4.1^d	65.3^c	0.003^a
50	5.0^c	68.4^c	0.003^a
100	7.4^a	82.5^a	0.002^b
200	6.8^b	76.6^b	0.003^b
SEM	0.1	1.0	0.00002
P-value	<0.001	<0.001	0.0007
^a-d Mean values in the same column with different superscript letters were significantly different (p<0.05). CAT, catalase; GSH-Px, glutathione peroxidase; MDA, malondialdehyde.

Table 6. Effects of dietary lycopene level (mg/ kg) on liver enzymes (U/L) in broilers
Treatments	AST	ALT	ALP

Control	387	5.3^a	4578^a
50	361	4.6^ab	4311^ab
100	352	4.1^b	4103^b
200	360	4.3^b	4128^b
SEM	7.4	0.2	87.9
p-value	0.1	0.02	0.04
^{a, b} Mean values in the same column with different superscript letters were significantly different (p<0.05). AST, aspartate amino transferase; ALT, alanine amino transferase; ALP, alkaline phosphatase.

The present study found that supplementation with lycopene significantly improved BWG and decreased FCR compared with control. Some reports indicated that lycopene improved the production characteristics of poultry compared with the control (Englmaierova et al 2011; Sahin et al 2006). Similar to results obtained in the present study, Englmaierova et al (2011) reported that dietary supplementation of chicken diets with lycopene increased BWG. In a study conducted in broilers, Sahin et al (2016) showed that dietary lycopene alleviates adverse effects of heat stress on performance. Lira et al (2010) showed that dietary supplementation of tomato waste that was high in lycopene significantly increased FI of broiler chickens. It was found that lycopene supplementation in Japanese quails diets improved BWG and FCR under heat stress conditions (Sahin et al 2006). On the contrary, Jain et al (1999) reported that supplementation of dietary lycopene did not affect BWG and FI in rat in thermoneutral conditions. On the basis of some reports a number of antioxidant compounds have been added into diets of broilers to improve growth performance (Tavarez et al 2011; Tawfeek et al 2014). Lycopene is a strong antioxidant with an ability to reduce harmful effects of ROS and oxidative damage to lipids, proteins, and DNA in the muscle (Rao and Agarwal 1999; Wang 2012). Therefore improvement in BWG and FCR in current experiment might be related to the antioxidant property of lycopene.

In the present study, lycopene supplementation decreased cholesterol, triglyceride and VLDL level in serum and increased the HDL amount. These results were in agreement with the study by Rao and Shen (2002), who observed a decrease in serum cholesterol in birds fed a diet enriched with lycopene. Sahin et al (2006) found that the inclusion of lycopene elevated HDL concentration and decreased LDL concentration in the blood plasma of Japanese quail. It has been shown that lycopene inhibitied cholesterol synthesis through preventing the hydroxyl-methylglutaryl-coenzyme A reductase enzyme (Fuhrman et al 1997).

Results in the present research indicate that lycopene supplementation might improve the activity of CAT and GSH-Px. Several useful effects of some micronutrients known as antioxidants have been reported (Angelo 1992; Rao and Agarwal 1999). Oxidative stress is an imbalance between the production of free radicals such as superoxide anion, hydrogen peroxide, and lipid peroxides and the ability of the body to deactivate their harmful effects by antioxidants (Fellenberg and Speisky 2006). The body is equipped with a variety of antioxidants that serve to neutralize the effect of free radicals. Antioxidants are divided into enzymatic and non-enzymatic groups. The major enzymatic antioxidants of the body are superoxide dismutase (SOD), CAT and GSH-Px (Evans and Halliwet 2001). The antioxidant status of animals can be determined by measuring total antioxidant capacity and activities of SOD and GSH-Px (Wang et al 2008). The CAT and SOD are antioxidant enzymes that directly react with free radicals. GSH-Px is an intracellular antioxidant enzyme that reduces the conversion of hydrogen peroxide to water to restrict its harmful effects (Sies 1999). Lycopene, a member of the carotenoid family and mainly found in tomato, is a strong antioxidant that prevents cell destruction caused by ROS (Agarwal and Rao 1998; Rao and Shen 2002). In the present study, the MDA production was significantly decreased by the addition of lycopene. The protective role of lycopene on the amount of MDA confirms the findings of other researchers (Rao and Agarwal 1999; Rao and Shen 2002). Similar to the results of the present study, Leal et al (1999) reported that supplementation of broilers diet with lycopene reduced the amount of MDA. Jain et al (1999) also showed that dietary lycopene decreased serum MDA concentration in rats. Sevcikova et al (2008) reported that the supplementation of chicken broiler diet with lycopene reduced oxidative stress markers such as MDA in breast muscles after 3 and 5 days of cold storage. The concentration of MDA in cultured cells and tissues reflects the antioxidant and lipid peroxidation status (Efe et al 1999). The level of MDA and activities of enzymes such as CAT and GSH-Px in tissues and organs are the important parameters for evaluation of oxidative stress status in birds (Salami et al 2015). Antioxidants in blood, cells and tissue fluids play an important role in reducing the rate of lipid oxidation and oxidative damage caused by the accumulated ROS (Saleh et al 2010). Lycopene is the strongest antioxidant among carotenoids, and is effective in reducing lipid oxidation and MDA production (Garcia et al 2009; Omoni and Aluko 2005).

Conclusion

The finding of the present study suggest that the supplementation of the diets with 100 mg lycopene could positively improve growth performance and antioxidative capacity of broiler chicks.

Acknowledgment

We thank the Lorestan University for its financial help

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Received 6 October 2018; Accepted 25 December 2018; Published 1 January 2019

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