doi:10.

1017/S0043933917001040

Lycopene: a natural antioxidant for

prevention of heat-induced oxidative
stress in poultry
M.A. ARAIN2, 3, †, Z MEI1†, F.U. HASSAN4, M. SAEED2, M ALAGAWANY5,
A.H. SHAR6 and I.R. RAJPUT1, 3*
1
College of Science Shantou University, Shantou, Guangdong, P.R. China;
2
Department of Animal Nutrition, College of Animal Sciences and Technology,
Northwest A&F University, Yangling, China, 712100; 3Faculty of Veterinary and
Animal Sciences, Lasbela University of Agriculture, Water and Marine Sciences,
Uthal, Balochistan, Pakistan 3800; 4Institute of Animal and Dairy Sciences, Faculty
of Animal Husbandry, University of Agriculture Faisalabad, Pakistan; 5Poultry
Department, Faculty of Agriculture, Zagazig University, 44511 Zagazig, Egypt;
6
College of Life Sciences, Northwest A&F University, Yangling, 712100, China
*Corresponding author: drimranrajput@gmail.com
†1st and 2nd author contributed equally

Heat stress is one of the most important physiological factors challenging poultry
production throughout the world especially in tropical and sub-tropical countries.
Oxidative stress induced by heat stress not only compromises productivity and
performance but also results in morbidity and mortality losses leading to the
economic burden for poultry producers. It reduces the shelf life of poultry
product in addition to poor meat and egg quality. Recently, a trend towards
using phytochemicals derived from natural sources with potential antioxidant
activities has increased. Lycopene is a predominant carotenoid pigment which is
universally found in fruits and vegetables, with tomatoes and their products being
key sources. Several in vivo and in vitro studies have suggested that lycopene is a
powerful antioxidant compared to other carotenoids. Supplementation of tomato
(Solanum lycopersicum) derived lycopene revealed numerous health promoting
activities in poultry birds, such as anti-oxidant, anti-inflammatory,
immunomodulation, improved performance and better meat as well as egg
quality. Lycopene maintains oxidative balance in birds through various ways
including serving as a free radical scavenger, inhibiting signalling pathways and
activating host antioxidant enzymes, such as superoxide dismutase (SOD),
glutathione peroxidase (GSH-Px) and catalase (CAT). The aims of this current
review are to summarise mechanisms of action through which lycopene quench
reactive species and maintain oxidative balance, highlight the potential role of
lycopene as a natural antioxidant agent for poultry industry and examine the

© World's Poultry Science Association 2017

World's Poultry Science Journal, Vol. 74, March 2018
Received for publication July 4, 2017
Accepted for publication October 18, 2017 1
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 Lycopene in poultry nutrition: M.A. Arain et al.

benefits to poultry producers when using this natural antioxidant on commercial

basis in poultry diets to alleviate the adverse effects of heat stress.

Keywords: heat stress; lycopene; antioxidant; poultry; oxidative stress

Introduction
Stress is a nonspecific response of a body to adverse stimuli, whereas any agent that
produces stress is known as a stressor (Selye, 1976). Therefore, any type of stress
exhibits a biological response or reaction to stimuli that adversely affect normal
physiological homeostasis. Several environmental factors, such as thermal irradiation,
air temperature, sunlight, humidity, and movement can cause this imbalance (Lara and
Rostagno, 2013). Heat stress in birds results in reduced feed intake and ultimately
reducing growth performance. Therefore, it has been an area of interest among
poultry producers and the scientific community for several decades, especially in
tropical, sub-tropical and arid parts of the world (Akbarian et al., 2016). A number of
physiological consequences associated with heat stress include decline in feed intake, rise
in body temperature, variable blood pH due to electrolyte imbalances, suppressed
immunity, alteration of reproductive and endocrine functions, less energy available for
cells, imbalances in digestibility and metabolism of several nutrients, disturbed gut
microflora and intestinal mucosa, and upregulated circulatory corticosterone and
cortisol levels (Lara and Rostagno, 2013; Renaudeau et al., 2012; Syafwan et al.,
2011; Yahav, 2009).
Recently, several studies revealed that heat stress induces oxidative stress, and
suppresses host anti-oxidant defence systems (Sahin et al., 2003; Sahin, 2015). Heat
stress decreases antioxidant status, which is one of the most important physiological
changes in response to high ambient temperature in poultry birds that increases oxidative
stress and immune suppression (Altan et al., 2003; Sahin et al., 2003; Lin et al., 2006;
Sahin, 2015). Increased levels of metabolites and radicals including nitrogen/reactive,
oxygen/chlorine species, collectively known as reactive oxygen species (ROS) under
stress poses serious physiological challenge as these substances are extremely reactive
and can alter cellular constituents, like lipids, proteins, and nucleic acids to induce
oxidative stress (Halliwell and Whiteman, 2004; Davies, 1995).
Recently, use of herbal plants and their phytochemicals have gained popularity in the
poultry industry to manage heat stress and improve the performance of poultry birds
(Saeed et al., 2015; 2017a; 2017b; 2017c; 2017d; 2017e; 2017f; Dhama et al., 2015).
Lycopene is a predominant carotenoid pigment which is universally found in fruits and
vegetables, with tomatoes and their products being key sources. Lycopene is one of the
carotenoids belonging to a family of compounds that are only found in microorganisms
and plants. It has great potential to maintain oxidative balance in host body through many
activities, including scavenging reactive oxygen species (ROS) or upregulating
production of antioxidant enzymes, such as superoxide dismutase (SOD), glutathione
peroxidase (GSH-Px) and catalase (CAT) (Martinez et al., 2008; Blokhina et al., 2003).
The health promoting and antioxidant potentials of lycopene have been known since
the late 1950s (Lingen et al., 1959; Lauretani et al., 2008). Because lycopene contains a
high amount of conjugated dienes, it has a scavenging ability which is twice than α-
tocopherol and ten times higher than β-carotene (Palozza et al., 2012a). A study
conducted by Sahin et al. (2008) revealed that lycopene-rich tomato powder
significantly improved feed intake, weight gain, and decreased concentration of

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 Lycopene in poultry nutrition: M.A. Arain et al.

malondialdehyde (MDA) in muscles, liver, and serum of Japanese quail reared under heat
stress. Sahin et al. (2006a; 2006b) reported similar effects of dietary lycopene on
antioxidant status and growth performance in heat stressed Japanese quails. Similarly,
in broilers under heat stress, dietary inclusion of lycopene-enriched tomato by-product at
a level of 5% in feed improved overall growth performance and, even at lower levels
(1%), enhanced total antioxidant capacity and lowered MDA level (Selim et al., 2013).
A few studies have reported that heat stress reduces production of antibodies and
relative weight of lymphoid organs (Lara and Rostagno 2013; Habibian et al., 2014).
However, there is limited literature is available on immunomodulatory effects of tomato-
derived lycopene in heat stressed birds, although broilers fed tomato puree have shown
improved antibodies titre against infectious bronchitis virus (IBV) and Newcastle disease
virus (NDV) in heat stressed conditions (Selim et al., 2013). The aim of this review is to
highlight the importance of lycopene and its enrich by-products as a potent treatment of
heat stress for poultry.

History, chemical structure and various sources of lycopene

Lycopene is a carotenoid extensively distributed in nature. Millared first time isolated it
in 1876 and named it ‘soanorubin’, while Schunk in 1903 again isolated it in pure form
and renamed it as lycopene (Vogele, 1937). Tomatoes, particularly deep red varieties, and
their by-products are richest sources of lycopene, although a few other fruits also contain
lycopene, such as guava, papaya, apricots, pink grapefruit and watermelon, as listed in
Figure 1 (Tanaka et al., 2012). Lycopene is a dark red colour pigment and waxy in nature
and it melts at 168°C whereby it changes into a crystal form.
Lycopene exists in ripe tomatoes as elongated needle-like crystals, with a molecular
formula of C40H56. Basically, it is an open chain polyene containing 13 double bonds
(Figure 1). Usually, lycopene is longer than other carotenoids and has no vitamin A-like
activity because of its symmetrical planarity (Srivastava and Srivastava, 2015).

Figure 1 Chemical structure and various source of lycopene.

World's Poultry Science Journal, Vol. 74, March 2018 3

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 Lycopene in poultry nutrition: M.A. Arain et al.

More than 700 carotenoids have been discovered so far, among which only 50 are
metabolisable in animals and lycopene is one of them (Srivastava and Srivastava, 2015).
The concentration of lycopene in various fruits and vegetables is shown in Figure 2 (Rao
and Agarwal, 1999; Anon, 2012).

Figure 2 Lycopene content in various food sources.

Effect of heat stress on immune response

Immune modulation is mediated through a complex system that involves endocrine,
nervous and immune systems. Recently several published studies have evaluated
responses under heat stress in poultry and suggested that heat stress suppresses
immunity and overall production performance (Bartlett and Smith, 2003; Niu et al.,
2009; Ghazi et al., 2012). Liver weight decreased when laying hens were exposed to
chronic heat stress (Felvergant et al., 2012), and Bartlett and Smith, (2003) reported that
immune biomarkers such as antibodies, IgG and IgM were downregulated in heat
stressed broilers. Aengwanich, (2010) observed a decline in weight of immune
organs, especially the bursa of Fabricius, with decreased numbers of circulating
lymphocytes in bursal regions in broilers under heat stress. Normally metabolic
attempts to maintain thermal homeostasis under high ambient temperatures produces
excessive ROS, and so the birds undergo oxidative stress physiologically, producing
antioxidant enzymes and heat shock proteins (HSP) to ameliorate adverse effects of
ROS (Droge, 2002). The elevated levels of HSP70 have been seen in laying hens and
broilers under heat stress (Marketon and Glaser, 2008; Gu et al., 2012).

Oxidative stress and lycopene

Lycopene protects cells and tissue damage caused by ROS (Palozza et al., 2011) and has
been ranked as more potent in this activity compared to other carotenoids such as α-

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 Lycopene in poultry nutrition: M.A. Arain et al.

tocopherol, ß-cryptoxanthin, β-carotene, lutein and zeaxanthin (Heber and Lu, 2002). The
most important biological role of lycopene is to protect DNA damage from oxidative
stress by oxygen-quenching and inhibiting mutation that can cause chronic diseases
(Goralczyk and Siler, 2003). Because of the elongated structure and conjugated
double bonds, lycopene is considered as the strongest free radical and single oxygen
scavenger among 600 naturally occurring carotenoids (Van Breemen and Pajkovic,
2008).
Lycopene mediates cell growth regulation, immune response, and modulation of phase
I and II detoxifying enzymes and gene transcription (Palozza et al., 2012b). It triggers
production of cellular enzymes, for example, glutathione S-transferase (GST), SOD, and
quinone reductase through the activation of so-called antioxidant response element
(ARE) (Van Breemen and Pajkovic, 2008; Sahin et al., 2011; 2013b). Many studies
have demonstrated that lycopene is a potent antioxidant agent to ameliorate adverse
effects of heat stress through several mechanisms (Table 1).
Several enzymes such as NQO1, GST, HO-1 and SOD are considered as antioxidant
and detoxifying enzymes also known as phase II cytoprotective enzymes. The promoter
regions of inducible genes encoding phase II enzymes contain ARE, which after binding
with Nrf2, leads to increased expression of these genes. Lycopene interrupts binding of
Nrf2/Keapl liberating Nrf2 which then transported to the nucleus and upregulate phase II
enzymes expression in heat stressed birds. Expression of NFκB is upregulated while
expression of Nrf2 is downregulated in birds under heat stress (Figure 3). In recent years,
several studies have proved that dietary lycopene predominantly work as an anti-stress
agent by triggering Nrf2/ARE transcription systems to alleviate oxidative stress and
maintain health in poultry (Table 1 and Figure 3). Treatment with lycopene rich
tomato powder downregulated activity and levels of NF-κB and correlated proteins
inhibiting inflammation in broilers exposed to heat stress (Sahin et al., 2011).

Figure 3 Regulation of NF-kB and Nrf2 signalling pathways by lycopene in heat-stressed poultry.

World's Poultry Science Journal, Vol. 74, March 2018 5

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 Lycopene in poultry nutrition: M.A. Arain et al.

Antioxidant effects of lycopene in broilers

Excessive heat causes oxidative stress in broilers which is a key factor that contributes to
decrease production performance and increase risk of pathological disorders (Mujahid et
al., 2005; 2007). Soybean and maize-based ingredients are generally used in diet
formulations, and these ingredients do not contain sufficient antioxidants required to
mitigate heat stress and oxidative stress. Therefore, dietary supplementation of
antioxidants like lycopene from alternative sources is often needed to ameliorate
oxidative stress. Studies in broilers showed that lycopene effectively enhanced levels
of antioxidant enzymes (SOD, GSH-Px) and significantly decreased MDA concentration
in muscles and serum. It modulated stress-related nuclear transcription factors in broilers
exposed to heat (Leal et al., 1999; Sahin et al., 2011; 2016). Dietary supplementation of
dried tomato pomace at the level of 5% enhanced growth performance, decreased HDL
cholesterol and triglycerides levels in broilers exposed to higher thermal temperature, and
activities of SOD and GPx improved while MDA concentration decreased (Hosseini-
Vashan et al., 2016). It has been reported that antioxidants derived from natural sources
quench free radicals, improve antioxidant enzyme activities and reduce lipid peroxidation
of AAPH-challenged broiler chicken erythrocyte cells (Zhang et al., 2014). In addition,
lycopene supplementation reduced cholesterol level in broiler meat (Englmaierová et al.,
2011).

Antioxidant effects of lycopene in layers

The adverse effects of high ambient temperature on the performance of laying hens have
been well documented which include deterioration of feed intake, egg quality, egg
production, egg weight and shell quality (Deaton et al., 1981; Marsden and Morris,
1987). Heat stress decreases the immunity status of birds through disruption of
synthesis of antibodies, ultimately increasing risk of diseases incidence leading to
morbidity and mortality losses (Zulkifli et al., 1994). Many studies have been
conducted on the effects of antioxidants like lycopene in layers and revealed that
dietary inclusion of pure lycopene or tomato powder not only improved oxidative
status of laying birds but also vitamin levels in circulating blood and egg yolk
(Karadas et al., 2006; Sahin et al., 2007; Olson et al., 2008; Akdemir et al., 2012).
Moreover, it was observed that dietary supplementation of tomato powder effectively
transferred carotenoid contents to egg yolk, which improved egg oxidative stability and
yolk colour (Akdemir et al., 2012). Similarly, in ovo inclusion of lycopene in hatching
eggs, improved day-old chick weight as well as organ weight index, while dietary
supplementation changed blood HDL cholesterol level and intestinal mucosal
development (Sun et al., 2015). Studies have demonstrated that dietary lycopene is a
potent antioxidant for enhancing the antioxidant defence in LPS-induced oxidative
stressed in laying hens and can improve egg quality and yolk colour (Yannakopoulos
et al., 1992; Dotas et al., 1999; Sun et al., 2014).

Antioxidant effects of lycopene in quail

Japanese quail (Coturnix coturnix Japonica) are commonly used as a suitable and
effective research model for other avian species (Minvielle, 2009; Ono et al., 2009).
Early studies evaluated antioxidant effects of lycopene in Japanese quails, which revealed
that lycopene enriched tomato powder mitigated heat stress through a reduction of MDA

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 Lycopene in poultry nutrition: M.A. Arain et al.

concentration in blood and liver (Sahin et al., 2008). The concentration of MDA in liver,
serum, and heart linearly decreased in quails with increasing dietary lycopene
supplementation (Sahin et al., 2006b; 2006c). Dietary supplementation linearly
improved oxidative stress markers such as Keap1expresion and Nrf2 expressions
(Sahin et al., 2013a). Additionally, a negative correlation was found between liver
MDA level and activities of antioxidant enzymes (Sahin et al., 2013b). Lycopene
supplementation at the level of 200 mg/kg ameliorated impairments induced by heat
stress and minimised the negative impact of stress in Japanese quail reared under high
ambient temperatures (Sahin et al., 2006c).

Conclusions
The poultry industry is facing numbers of challenges, especially in tropical and
subtropical countries, to prevent oxidative stress-related issues posed by heat stress in
a competitive price and quality consumer market. Lycopene is one of the powerful
promising natural antioxidants that can mitigate adverse effects of heat stress. Several
in vitro, animal, and human studies have shown that lycopene induces anti-stress
activities through many ways including quenching of ROS, induction of phase II
cytoprotective enzymes and inhibition of several signalling pathways. Current studies
reviewed have shown that lycopene possesses anti-stress properties however, further
research on a molecular basis are needed to find out the molecular mechanism in
various poultry models to validate the usefulness of lycopene as a potent antioxidant
agent.

Conflict of interests
There were no conflicts of interests.

Acknowledgment
All the authors of the manuscript thank and acknowledge their respective Universities
and Institutes.

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Table 1 A summary of studies with lycopene on heat stress related cellular activities in various poultry species.

Study model Housing Condition Treatment and Results Mechanism of action References
Doses

Broiler chicks 22°C for 24 h/d (TN) Basal diet + 0, 200 ↑muscle Keap1, muscle Nrf2 Regulating NF-kB and Nrf2 Sahin et al.
or 34°C for 8 h/d (HS) or 400 mg/kg ↓muscle MDA pathway Antioxidant activity (2013b)
lycopene ↑Muscle lycopene levels and activities of
SOD and GSH-Px

Japanese 22°C for 24 h/d or Basal diet + 25 or ↓liver NF-κB levels Regulating NF-kB and Nrf2 Sahin et al.
World's Poultry Science Journal, Vol. 74, March 2018

quails 34°C for 8 h/d 50 g/kg tomato ↑liver Nrf2 levels pathway Antioxidant activity (2011)
powder ↓liver MDA levels
↑liver SOD, CAT, GSH-Px activities

Japanese 22°C or 34°C for 8 h/d Basal diet + 2.5 or ↓oxidative stress markers Modulates the oxidation- Sahin et al.
quail 5.0% of tomato ↓MDA levels antioxidation system (2008)

Lycopene in poultry nutrition: M.A. Arain et al.

powder

Laying hens Temperature- Basal diet + 5 or 10 ↑concentrations of serum and egg yolk Antioxidant activity Akdemir
controlled g/kg tomato lycopene, β-carotene, lutein and vitamin A et al. (2012)
powder ↓MDA levels

Japanese 22°C or 34°C Basal diet + 50, 100 ↓serum liver, and heart MDA levels Modulates the oxidation- Sahin et al.
quail or 200 mg/kg ↓serum cholesterol, triglycerides and antioxidation system (2006b)
lycopene glucose concentrations

Broilers Temperature- Basal diet + 0 and ↑oxidative stability Modulates the oxidation- Englmaierová
controlled 75 mg/kg lycopene antioxidation system et al. (2011)

Broiler Temperature- Basal diet + 50 or ↓Concentration of MDA Modulates the oxidation- Ševcíková
cockerels controlled 100 mg/kg antioxidation system and Skřivan
lycopene (2008)
11
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12

Lycopene in poultry nutrition: M.A. Arain et al.

Table 1 Continued

Study model Housing Condition Treatment and Results Mechanism of action References
Doses
World's Poultry Science Journal, Vol. 74, March 2018

Broilers 22°C for 24 h/d (TN) Basal diet + 0, 200, ↓Keap1 expression Regulating Keap1 and Nrf2 Sahin et al.
or 34°C for 8 h (HS) or 400 mg/kg ↑Nrf2 expression pathway and antioxidant (2016)
lycopen ↑serum an muscle SOD and GSH-Px activities activity
↑serum an muscle SOD and GSH-Px activities
↓ Concentration of MDA

Broilers 21°C for 24 h/d and 21 Basal diet + 5% ↓Triglycerides Modulates the oxidation- Hosseini-
to 34°C for 9 h (HS) lycopene/kg ↑GPx and SOD ALT, AST, ALP, and lipase antioxidation system Vashan et al.
concentration Immune modulation (2016)
↓ Concentration of MDA

Breeding Temperature- Basal diet + 0, 20, ↑ HDLC, T3, GSH/GSSG Modulates the oxidation- Sun et al.
hens controlled 40, or 80 mg/kg ↑immune organ index antioxidation system (2014)
diet lycopene ↓ LDLC Immune modulation

Breeder Temperature- Basal diet + (0-40 ↑chick birth body weight Modulates the oxidation- Sun et al.
laying hens controlled mg/kg lycopene ↑Liver antioxidant capacity, GSH-Px and antioxidation system (2015)
GSH: GSSG Immune modulation
↓ concentration of MDA

Japanese 22°C (TN) or 34°C for Basal diet + 50, 100 ↓VLDL and LDL Modulates the oxidation- Sahin et al.
quail 12 h/day (HS) or 200 mg /kg ↑HDL antioxidation system (2006a)
lycopene

Japanese 20 ± 2.5°C. Basal diet + (0-100 ↓Serum and liver MDA Modulates the oxidation- Sahin et al.
quail mg/kg lycopene ↓serum and yolk cholesterol level antioxidation system (2006b)
↑antioxidant status
↑: increase, ↓: decrease, TN: thermo-neutral, HS: heat stress, MDA: malondialdehyde, SOD: Superoxide dismutase, ALT: Alanine transaminase, AST: Aspartate transaminase,
ALP: Alkaline phosphatase, HDLC: high density lipoprotein cholesterol, T3: triiodothyronine, GSH/GSSG: reduced glutathione to oxidised glutathione ratio, VLDL: Very-
low-density lipoprotein, LDL: low-density lipoprotein, HDL: high -density lipoprotein.