Tomato powder in laying hen diets: Effects on concentrations of yolk carotenoids and lipid peroxidation

Abstract

1. The effects of tomato powder supplementation on performance, egg quality, serum and egg yolk carotenoids, vitamins and malondialdehyde (MDA) concentrations in were investigated in laying hens in mid-lay. 2. A total of 90 laying hens, 49 weeks old, were divided into 3 groups consisting of 6 replicate cages, 5 birds per cage. Birds were randomly fed on one of three diets: basal diet and basal diet added with 5 or 10 g tomato powder per kg diet. 3. As tomato powder concentration increased, there were linear increases in feed intake, egg production, egg weight and yolk colour and a linear decrease in feed conversion. Shell weight, shell thickness and Haugh unit remained unchanged in response to dietary treatments. 4. Concentrations of serum and egg yolk lycopene, β-carotene, lutein and vitamin A increased for both diets including tomato powder, whereas MDA decreased linearly with increasing supplemental tomato powder concentration. 5. Tomato powder supplementation increased egg production persistency and increased carotenoids and vitamin A contents in egg yolk, accompanied by reduced yolk lipid peroxidation.

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Tomato powder in laying hen diets: effects on
concentrations of yolk carotenoids and lipid
peroxidation
F. Akdemir a , C. Orhan b , N. Sahin b , Dr K. Sahin a & A. Hayirli c
a Department of Animal Nutrition, Faculty of Veterinary Medicine, Dicle University,
21280 Diyarbakir, Turkey
b Department of Animal Nutrition, Faculty of Veterinary Medicine, Firat University, 23119
Elazig, Turkey
c Department of Animal Nutrition, Faculty of Veterinary Medicine, Atatürk University,
25240 Erzurum, Turkey
Accepted author version posted online: 24 Sep 2012.Version of record first published: 03
Jan 2013.
To cite this article: F. Akdemir , C. Orhan , N. Sahin , Dr K. Sahin & A. Hayirli (2012): Tomato powder in laying hen diets:
effects on concentrations of yolk carotenoids and lipid peroxidation, British Poultry Science, 53:5, 675-680
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British Poultry Science Volume 53, Number 5 (October 2012), pp. 675
—
680
Tomato powder in laying hen diets: effects on concentrations of yolk
carotenoids and lipid peroxidation
F. AKDEMIR, C. ORHAN
1
, N. SAHIN
1
, K. SAHIN AND A. HAYIRLI
2
Department of Animal Nutrition, Faculty of Veterinary Medicine, Dicle University, 21280 Diyarbakir, Turkey,
1
Department of Animal Nutrition, Faculty of Veterinary Medicine, Firat University, 23119 Elazig, Turkey, and
2
Department of Animal Nutrition, Faculty of Veterinary Medicine, Atatu¨rk University, 25240 Erzurum, Turkey
Abstract 1. The effects of tomato powder supplementation on performance, egg quality, serum and
egg yolk carotenoids, vitamins and malondialdehyde (MDA) concentrations in were investigated in
laying hens in mid-lay.
2. A total of 90 laying hens, 49 weeks old, were divided into 3 groups consisting of 6 replicate cages, 5
birds per cage. Birds were randomly fed on one of three diets: basal diet and basal diet added with 5 or
10 g tomato powder per kg diet.
3. As tomato powder concentration increased, there were linear increases in feed intake, egg
production, egg weight and yolk colour and a linear decrease in feed conversion. Shell weight, shell
thickness and Haugh unit remained unchanged in response to dietary treatments.
4. Concentrations of serum and egg yolk lycopene, -carotene, lutein and vitamin A increased for both
diets including tomato powder, whereas MDA decreased linearly with increasing supplemental tomato
powder concentration.
5. Tomato powder supplementation increased egg production persistency and increased carotenoids
and vitamin A contents in egg yolk, accompanied by reduced yolk lipid peroxidation.
INTRODUCTION
Carotenoids are pigmented phytochemicals
responsible for red, yellow and orange colours
of fruits and vegetables (Mangels et al., 1993; Rao
and Agarwal, 1999). Tomato, one of the carote-
noid-rich fruits, contains large quantities of
lycopene (80
—
90% of total carotenoids), -caro-
tene (7
—
10%) and smaller quantities of lutein,
-carotene, g-carotene, -carotene, violaxanthin,
zeaxanthin, neoxanthin, -cryptoxanthin, -cryp-
toxanthin, neurosporene, phytoene, phytofluene,
cyclolycopene and some other beneficial mole-
cules such as vitamin E, vitamin C and flavonoids
(Bourne and Rice-Evans, 1998; Nguyen and
Schwartz, 1999; Khachik et al., 2002; Burns
et al., 2003). Lycopene possesses a powerful
antioxidant activity, protects cells/tissues from
the oxidative damage caused by reactive oxygen
species (Di-Mascio et al., 1989; Rao and Shen,
2002). In association with these properties, lyco-
pene has been shown to play an important role in
preventing certain types of cancer, cardiovascular
and degenerative diseases, improving gene regu-
lation, gap-junction communications, immune
functions and hormonal and metabolic pathways
(Zhang et al., 1991; Gerster, 1993; Meydani et al.,
1995; Mayne, 1996; Aust et al., 2003; Rao et al.,
2006). Other useful compounds present in
tomato such as -carotene, lutein and flavonoids
also exert antioxidant effects (Hertog et al., 1993;
Khachik et al., 1995; Mayne, 1996).
Acceptability of foods of animal origin is a
very important factor in human nutrition
(Angelo, 1992; Flachowsky et al., 2002). Some
phytochemicals, such as isoflavones, polyphenols
Correspondence to: Dr Kazim Sahin, Department of Animal Nutrition, Faculty of Veterinary Science, Firat University, 23119 Elazig, Turkey.
E-mail: nsahinkm@yahoo.com
Accepted for publication 30th May 2012.
ISSN 0007–1668(print)/ISSN 1466–1799 (online)/12/050675
—
6ß2012 British Poultry Science Ltd
http://dx.doi.org/10.1080/00071668.2012.729142
Downloaded by [Inonu Universitesi] at 22:26 03 January 2013

and carotenoids, are added to animal diets to
improve product quality with respect to colour,
tenderness, oxidative stability and storage prop-
erties (Hertog et al., 1993; Adlercreutz, 1995;
Rock et al., 1996; McCall and Frei, 1999). These
beneficial phytochemicals can easily pass into
and accumulate in the animal food product
(Leeson and Caston, 2004; Cachaldora et al.,
2008; Sahin et al., 2008a; Akdemir and Sahin,
2009; Sahin et al., 2010). Therefore, the objective
in this study was to determine the effect of
dietary tomato powder supplementation on per-
formance, egg quality and lipid peroxidation in
mid-lay hens.
MATERIALS AND METHODS
A total of 90 49-week-old white laying hens
(Lohman LSL, hybrid) were used in accordance
with animal welfare regulations at the Umut
Tavukculuk of Elazig, Turkey. Hens were
assigned randomly to one of three groups. Each
treatment consisted of 6 replicate cages of 5 birds
per cage. The birds were housed in wire cages
and exposed to a 16 L:8D illumination cycle.
Feed and fresh water were offered ad libitum
throughout the experiment.
After a 10-d adaptation period, birds were
given diets containing 0, 5 or 10 g tomato powder
per kg diet for a period of 90 d. Tomato powder
(Natural Carotenoid Biomass with Lycopene
Õ
,
Vitan Ltd., Dneprovsky, Ukraine) contained 11%
protein and 6% lycopene. Experimental diets
(Table 1) were stored in black plastic containers
at 4C to avoid photo-oxidation. Feed consump-
tion was measured weekly and egg production
rate and egg weights were recorded daily. At the
end of the study, egg quality parameters (egg
weight, yolk colour, yolk weight, shell weight,
shell thickness and Haugh unit) were measured
on two eggs collected randomly from each of 6
replicates per group. Egg yolk colour was deter-
mined by using the Roche Color Fan according to
the CIE standard colorimetric system. Haugh
units were calculated using following formula:
Haugh unit ¼100x log (H þ757
—
17x W
037
)
where H ¼albumen height, mm and W ¼egg
weight, g (Eisen et al., 1962) after determining
albumen height by a micrometer (Saginomiya,
TLM-N1010, Japan) and egg weight.
Feed samples were analysed in triplicate for
crude protein (#98805), ether extract (#93206),
crude fibre (#96209), crude ash (#93607), Ca
(#96808) and P (#96517) (AOAC, 1990). Energy
and amino acid (methionine and lysine) contents
were calculated from tabular values listed for the
feedstuffs (Jurgens, 1996). A total of 12 eggs from
each group were collected randomly and yolks
were separated from albumen. For serum
analysis, blood samples were collected from the
axillary vein of two hens from each of 6 cages per
group. Yolk and serum samples were subjected to
duplicate analyses for carotenoids (lycopene,
-carotene and lutein) (Stahl and Sies, 1992),
vitamins (A and E) (Mori et al., 2003) and MDA
(Karatepe, 2004) using high performance liquid
chromatography (HPLC, Shimadzu, Kyoto,
Japan). All-trans-retinol and -tocopherol were
used as standards (Sigma Chemical Co., St Louis,
MO). The equipment for HPLC consisted of a
pump (LC-20AD), a Diode Array Detector (SPD-
M10A) for carotenoids, vitamins and MDA, a
column oven (CTO-10ASVP), an autosampler
(SIL-20 A) a degasser unit (DGU-20A5), column
(Inertsil ODS-3, 250x 46 mm, 5 mm) and a com-
puter system with LC solution Software
(Shimadzu, Kyoto, Japan).
In sample size calculation, 10% improvement
in egg lycopene concentration was considered to
be significant at type I error of 005 with the
power of 085. Data were subjected to one-way
ANOVA using the PROC MIXED procedure of
Statistical Analysis System (SAS, 1999). Linear
model to test effects of dietary tomato powder
supplementation on animal performance and
egg quality was y
ij
¼mþb
0
þL
i
þe
j
, where
y¼response variable, m¼population mean,
Table 1. Ingredient and nutrient composition of the
basal diet
a
Ingredient g/kg
Maize 6300
Soybean meal 1958
Meat-bone meal 500
Soy oil 227
Limestone 890
Dicalcium phosphate 25
Vitamin-mineral premix
b
60
Sodium chloride 20
Sodium bicarbonate 20
Chemical analyses (g/kg, dry matter basis)
c
Metabolisable energy, MJ/kg 1176
Crude protein 170275
Crude fat 45024
Crude fibre 35213
Crude ash 120860
Calcium 40017
Phosphorus 35018
Methionine 46
Lysine 91
a
Tomato powder was added into diets at expense of maize.
b
Supplied per kg of diet: retinyl acetate, 4128 mg; cholecalciferol, 60 mg;
dl--tocopheryl acetate, 30 mg; menadione sodium bisulphite, 25 mg;
thiamine-hydrochloride, 3 mg; riboflavin, 7mg; niacin, 40 mg; d-pantothe-
nic acid, 8 mg; pyridoxine hydrochloride, 4 mg; vitamin B
12
,0015 mg;
vitamin C, 50 mg; folic acid, 1 mg; D-biotin, 0045 mg; choline chloride,
125 mg; Mn (MnSO
4
-H
2
O), 80 mg; Fe (FeSO
4
-7H
2
O), 30 mg; Zn (ZnO),
60 mg; Cu (CuSO
4
-5H
2
O), 5 mg; Co (CoCl
2
-6H
2
O), 01 mg; I as KI, 04 mg;
Se (Na
2
SeO
3
), 015 mg.
c
Metabolisable energy, methionine and lysine are calculated based on
tabular values for feedstuffs (Jurgens, 1996). Others are mean of 3
replicates.
676 F. AKDEMIR ET AL.
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b
0
¼covariate, L¼tomato powder supplementa-
tion and e¼residual error being N(0, 1). Egg
production and egg weight data during the
adaptation period were used as covariates for
corresponding response variables. The model
also included orthogonal and polynomial con-
trasts to determine tomato powder supplemen-
tation effects and changes in response variable
with increasing dietary tomato powder
supplementation. Statistical significance was
declared at P<005.
RESULTS
The mean egg production (9333 034%) and
egg weight (6210 013 g) was similar in all
groups during the adaptation period. Hens
receiving diets supplemented with tomato
powder had greater feed intake, egg production
and egg and yolk weights, darker yolk colour and
more efficient feed conversion than hens not
supplemented with tomato powder (Table 2).
As dietary tomato powder concentration
increased, feed intake (P<001), egg production
(P<0001) and egg (P<001) and yolk (P<001)
weights and yolk colour (P<00001) linearly
increased and feed efficiency (P<005) linearly
increased (Table 2; Figure). The dietary
treatments did not affect shell weight, shell
thickness or Haugh units.
Serum and egg yolk lycopene and -carotene
concentrations were influenced by tomato
powder concentrations (Table 3). Serum and
egg yolk lycopene, -carotene, lutein and vitamin
A concentrations increased for hens given diets
supplemented with tomato powder (Table 3).
The same was true for serum vitamin E concen-
trations whereas yolk vitamin E concentration
did not differ between treatments (Table 3).
Table 2. Effects of tomato powder supplementation to hen diets on performance and egg quality (ls-means over a 90-d period)
Variable Tomato powder, g/kg SEM Statistical significance, P<
a
0 5 10 S L Q
Feed intake, g/d 1149 1155 116302001 0001 NS
Egg production
b
,% 8994 9139 9311 035 0001 00001 NS
Feed consumption
c
202 196 186 002 005 001 NS
Egg weight
d
,g 6373 6455 6659 042 001 001 NS
Shell weight, g 649 679 697 010 014 005 NS
Shell thickness, mm 0398 0399 0393 0004 NS NS NS
Haugh unit
e
8792 8940 8808 087 NS NS NS
Egg yolk colour 1125 1308 1358 026 00001 00001 NS
Egg yolk weight, g 1638 1659 1711 016 001 001 NS
a
Statistical contrast: S ¼Tomato powder supplementation effect (hen supplemented with tomato powder vs hen not supplemented with tomato powder);
L¼Linear effect of increasing dietary tomato powder; Q ¼Quadratic effect of increasing dietary tomato powder. NS ¼not significant.
b
n¼6 cages, 5 birds per cage.
c
g feed consumed per g egg mass (egg number x egg weight).
d
n¼12 eggs per group.
e
Haugh unit ¼100x log(Hþ757
—
17x W
037
) where H¼albumen height, mm and W¼egg weight, g.
85
86
87
88
89
90
91
92
93
94
95
Covariate 1-15 days 16-30
days
31-45
days
46-60
days
61-75
days
76-90
days
Time relative to ex
p
eriment, two weeks
Egg production, %
Figure. Effects of tomato powder (f, 0 g/kg; #, 5 g/kg; m, 10 g/kg) supplementation on egg production. Covariate is average initial
egg production of all birds first 10 d prior to the experimental period at the age of 49 weeks.
TOMATO POWDER FOR LAYING HENS 677
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Hens fed on a diet with tomato powder had
lower serum and egg yolk MDA concentrations
than hens on a diet without tomato powder.
There were linear increases in serum and yolk
lycopene, -carotene, lutein and vitamin A con-
centrations and decreased MDA concentrations
in serum and yolk as tomato powder concentra-
tion in the diet increased. Despite no changes in
yolk vitamin E concentration, its concentration
in serum linearly increased with increasing die-
tary tomato powder concentration.
DISCUSSION
This experiment tested whether tomato powder
supplementation to mid-lay hens improve per-
formance and egg quality in terms of reducing
lipid peroxidation through enriching it with
vitamins and carotenoids possessing antioxidant
properties. Acceptability of foods of animal
origin by consumers is influenced by quality
factors such as colour, tenderness, oxidative
stability and storage properties (Angelo, 1992;
Herber and Van Elswyk, 1998; Flachowsky et al.,
2002). It is well known that enrichment of poultry
diets with carotenoids results in increased con-
centration in the egg yolk. Pure lycopene or
lycopene-rich vegetables such as tomato or
tomato by-products have been studied to obtain
the darkest egg yolk colour and stable eggs
resulting from their increased antioxidant ability
against lipid peroxidation (Knoblich et al., 2005;
Karadas et al., 2006a; Olson et al., 2008; Sahin
et al., 2008a). Lycopene is a predominant
carotenoid that gives red colour to tomatoes
(Rao and Agarwal, 1999). It is a strong antioxi-
dant and potently reduces oxidative damages of
lipids, proteins and DNA (Di-Mascio et al., 1989;
Rao and Agarwal, 1999). In agreement with the
present data, other studies in which lycopene or
lycopene-rich tomato byproducts were supple-
mented to poultry diets resulted in increased egg
yolk colour darkness (Knoblich et al., 2005;
Karadas et al., 2006a; Mansoori et al., 2008;
Olson et al., 2008). Moreover, in response to
tomato powder supplementation, increased egg
yolk lycopene concentration was associated with
decreased egg yolk MDA concentrations, sug-
gesting that enrichment of diets with vitamins
and carotenoids reduced egg yolk lipid peroxi-
dation (Karadas et al., 2006a,b; Olson et al., 2008;
Sahin et al., 2008a). It is well documented that
lycopene and vitamin E synergistically inhibit
TBARS formation, another lipid peroxidation
indicator (Shixian et al., 2005; Sahin et al., 2006b).
Furthermore, Alshatwi et al. (2010) declared that
tomato powder was more protective than lyco-
pene against lipid peroxidation in rats. An
inverse association between serum lycopene
and MDA was also shown in this study and
others (Sahin et al., 2006a, 2007, 2008b).
Other carotenoids in tomato powder such as
lutein and -carotene also exert biological and
antioxidant activities (Khachik et al., 1995;
Mayne, 1996). In the present study, lutein and
-carotene concentrations in serum and egg yolk
of hens given feed supplemented with tomato
powder were significantly higher than control
group. Other studies also noted that serum lutein
and -carotene concentrations increased when
quails were given feed supplemented with
Table 3. Effects of tomato powder supplementation to hen diets on serum-egg yolk carotenoid, vitamin and MDA levels (ls-means over
a 90-day period)
Variable Tomato powder, g/kg SEM Statistical significance, P<
a
0 5 110 S L Q
Serum
b
,mg/ml
Lycopene ND 1389 1669 051 00001 00001 00001
-carotene 3721 1230 152912000001 00001 005
Lutein 166 301 323 020 0001 0001 NS
Vitamin A 154 257 334 038 005 001 NS
Vitamin E 599 830 1017 071 001 0001 NS
Malondialdehyde 0198 0150 0121 0017 001 001 NS
Egg yolk
c
,mg/g
Lycopene ND 653 805 0195 00001 00001 00001
-carotene 1720 3310 551323600001 00001 NS
Lutein 685 723 903 032 0001 00001 NS
Vitamin A 1043 1081 1211 039 005 001 NS
Vitamin E 1372 1412 1434105NS NS NS
Malondialdehyde 0335 0248 0211 0015 00001 00001 NS
a
Statistical contrast: S ¼Tomato powder supplementation effect (hen supplemented with tomato powder vs hen not supplemented with tomato powder);
L¼Linear effect of increasing dietary tomato powder; Q ¼Quadratic effect of increasing dietary tomato powder. NS ¼not significant.
b
n¼12 hens per group.
c
n¼12 eggs per group.
678 F. AKDEMIR ET AL.
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tomato powder (Karadas et al., 2006a,b; Sahin
et al. 2007). Tomato powder supplementation to
diets increased serum and yolk carotenoids and
vitamin A concentrations. Vitamin E concentra-
tions were increased in serum, but not yolk
(Table 3). Previous studies investigating tomato
powder or pure lycopene supplementation
showed increase in both vitamins in serum and
egg yolk (Karadas et al., 2005, 2006b; Sahin et al.,
2006a,b, 2007, 2008b; Olson et al., 2008).
In disagreement with the present study
(except for egg weight), Jafari et al. (2006) and
Mansoori et al. (2008) achieved the improve-
ments in quality parameters (Haugh unit, shell
weight, shell thickness and egg weight) in laying
hen supplemented with diets containing dried
tomato pomace and tomato pulp. Sahin et al.
(2008a), however, reported that egg weight and
feed conversion were not affected by lycopene
supplementation.
In conclusion, carotenoids were effectively
transferred from the diet to the egg yolk via
tomato powder supplementation to mid-lay hen
diets, which resulted in improvements in egg yolk
colour and oxidative stability. That is, natural
supplements rich in beneficial phytochemicals
can be added at up to 10 g per kg to poultry diets
to improve egg quality.
ACKNOWLEDGEMENTS
The authors thank Vitan Ltd. (Dneprovsky, Ukraine)
for providing tomato powder and the Umut
Tavukculuk San. Tic. A.S. for allowing us to use
their facility.
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