Journal of Animal and Feed Sciences, 30, 2021, 367–378     https://doi.org/10.

22358/jafs/143104/2021
The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Jabłonna

Effect of hesperidin addition to quail diets on fattening

performance and quality parameters, microbial load,
lipid peroxidation and fatty acid profile of meat

A. Özbilgin1, K. Kara2,4 and S. Urçar Gelen3

1
Sivas Cumhuriyet University, Faculty of Veterinary Medicine, Department of Animal Nutrition and Nutritional Diseases,
58140, Sivas, Turkey
2
Erciyes University, Faculty of Veterinary Medicine, Department of Animal Nutrition and Nutritional Diseases,
38280, Kayseri, Turkey
3
Atatürk University, Faculty of Veterinary Medicine, Department of Food Hygiene and Technology, 25240, Erzurum, Turkey

KEY WORDS: fatty acids, hesperidin, lipid ABSTRACT. This study examines the effect of different doses of hesperidin
peroxidation, meat quality, microbial count, added to quail diets on growth performance of birds as well as on lipid
quails peroxidation, some microbiological and physicochemical properties, and fatty
acid profile of thigh tissue. In total 300 (male and female) Japanese quail
(Coturnix coturnix japonica) were divided into three groups: control (C) group
fed only a basal diet, HES1 and HES2 groups fed basal diet with the addition
of 1 and 2 g/kg hesperidin, respectively. It was observed that hesperidin
addition to quail diets had no effect on the growth performance parameters,
Received: 21 May 2021 such as live weight, feed consumption and feed conversion ratio, regardless
Revised: 17 August 2021 of examined dose. It was determined that hesperidin dose did not affect meat
Accepted: 15 October 2021 water activity (P > 0.05) but influenced pH or colour parameters [brightness
(L*), redness (a*), yellowness (b*)] of meat (P < 0.05). Furthermore, the
antibacterial effect of hesperidin supplementation was observed as counts of
total mesophilic bacteria, Enterobacteriaceae, Lactobacillus spp., Lactococcus
spp., Micrococcus/Staphylococcus and total psychrophilic aerobic bacteria
were limited and variable (P < 0.05). It was determined that hesperidin had
a statistically significant effect on lipid peroxidation in meat on day 1 and 4 of
storage. In addition, it was observed that the added hesperidin had a positive
effect on n-3 polyunsaturated fatty acids (PUFA; such as α-linolenic acid,
eicosapentaenoic acid and docosahexaenoic acid) in terms of the lipid profile
in thigh tissue (P < 0.05). So, it can be concluded that the hesperidin addition to
quail diets exerted influence on microbiological properties and lipid peroxidation
4
Corresponding author: of meat, which can influence shelf life quality of quail meat; but also hesperidin
e-mail: [email protected] addition had a health-promoting effect on the fatty acid profile of thigh meat
increasing n-3 PUFA content.

Introduction deterioration of the colour, smell and taste of meat

due to oxidation processes (Engberg et al., 1996).
Poultry meat has many desirable nutritional Cells are susceptible to oxidation due to the prop-
properties due to its low-fat and high-unsaturated erties of membrane phospholipids and their high
fatty acid contents (Simopoulos, 2000). However, content of unsaturated fatty acids, which leads to
a high unsaturation of fatty acid in tissue can lead to the formation of secondary products of oxidation
368 Hesperidin addition to quail diets

reactions, such as short-chain aldehydes, ketones hesperidin, which is added to the diet at varying rates,
or hydroperoxides. These compounds can adverse- changes the pH of the meat, also of quail meat (Nasr
ly affect lipids, pigments, proteins, carbohydrates et al., 2017). Also it was reported that addition of
and vitamins, and consequently, result in the loss hesperidin to the diet reduces the malondialdehyde
of important features, such as the meat flavour, co- (MDA) – lipid peroxidation indicator – concentra-
lour, nutritional value and quality, which limits the tion in meat (examined hesperidin doses: 1.5–3 g/kg;
shelf life of the product (Maraschiello et al., 1998; Simitzis et al., 2011; Kamboh and Zhu, 2013). The
Sárraga and García-Regueiro, 1999). Flavonoids possible positive effects of adding hesperidin to the
usually contain one or more aromatic hydroxyl diet in terms of meat microbial load have been deter-
groups that reduce free radicals and are responsible mined until now only in in vitro studies (Karayıldırım,
for antioxidant activity. They are commonly found 2017; Ambrosio et al., 2020).
in plant products as secondary metabolites, synthe- Therefore the aim of the present study was to de-
sized for defense against ultraviolet light, physical termine how different doses of hesperidin addition to
damage, stress, pathogens and infections (Robbins, the quails diets will affect fattening performance of
2003). Flavonoids, and especially the subgroup of birds, meat quality parameters (microbiological and
flavanones containing hesperidin and naringin that physicochemical properties (colour) and fatty acid
are well known for their antioxidant properties, have profile) as well as lipid oxidation in meat depending
multifactorial activities and are compounds that as- on the storage period.
sure health to living organisms (Erlund, 2004).
Green tea, rosemary and grape pulp, which are
rich in phenolic substances with antioxidant activity,
Material and methods
have been added to poultry rations as raw materials
and extracts (Smet et al., 2008; Kara et al., 2016a,b,c; Animals, experiment schedule and diets
2021). In recent years, there have been more and This study was conducted with the permission
more attempts to add by-products, especially from of the Sivas Cumhuriyet University, Animal Ex-
citrus fruits, to animal diets. Citrus pulp is obtained periments Local Ethics Board, dated 2019 and num-
after removing the juice from the fruit and is there- bered 253.
fore a mixture of citrus peels, their insides, and part In the study, 300  quails (Coturnix coturnix
of the peel. Citrus pulp and residues are widely used japonica) of mixed sex, aging 10–15  days were
in animal feeding. They have a positive impact on ex- housed in cages (20  quails per cage) with dimen-
pensive waste management programmes prevention. sions of 20 × 45 × 100  cm in a closed area at the
Fibres obtained from citrus fruit pulp have an addi- Sivas Cumhuriyet University, Faculty of Veterinary
tional advantage: they contain bioactive compounds Medicine for a one-week adaptation period and then
(flavonoids)  – functional components providing 5  weeks of experimental period. Animals were dis-
health benefits as mentioned above. Bioflavonoids tributed without causing a  statistical difference be-
such as hesperidin and naringenin are abundant as an tween the control and trial groups in terms of average
inexpensive by-product of citrus cultivation. live weight values. In the experiment, the birds were
Hesperidin is a naturally occurring polyphenolic divided into 3  groups of 100 birds each, and each
compound widely distributed in the plant kingdom group was divided into 5 repetition, 20 quails each.
as a  secondary metabolite. Hesperidin is a  flava- The groups were: control (C) fed only basal diet;
none glycoside comprising an aglycone, hesperitin HES1 group fed the basal diet + 1 g/kg of hesperidin;
or methyl eriodictyol and an attached disaccharide, HES2 group fed the basal diet + 2 g/kg of hesperi-
rutinose (Garg et al., 2001). Pure hesperidin occurs din. Hesperidin (C28H34O15, cas no: 520-26-13, purity
as long hair-like needles, yellow in colour. It is taste- grade 91%, Chem-Impex Int. Company, Wood Dale,
less and odourless. A deficiency of this substance in IL, USA) was obtained from the market as purified
human diet has been linked with abnormal capillary from orange fruit. Doses were formulated according
leakage as well as pain in the extremities causing to Goliomytis et al. (2015). In the study, animals had
aches, weakness and leg cramps (Garg et al., 2001). ad libitum access to feed and water. All animals ex-
There are many studies on adding flavonoids ex- perienced a comfortable temperature (22–24 °C) and
tracted from citrus fruits to poultry diets and its effect 23/1 h daylight/darkness per day. Animal diets were
on live weight changes (Simitzis et al., 2011; Hajati formulated according to the recommendations of
et al., 2012; Goliomytis et al., 2014, 2015). The ad- the National Research Council (NRC, 1994) and the
dition of Gingko biloba extract in varying doses has chemical analysis of diets was performed according
been also tested (Cao et al., 2012). It was found that to the AOAC Internationl (2000) (Table 1).
A. Özbilgin et al. 369

Table 1. Composition of basal and experimental diets Quality characteristics of the meat
Indices
Diet1 Twenty five-gram samples of the thigh meat tak-
C HES1 HES2 en from slaughtered birds was covered with stretch
Feed raw materials, % wrap on polyethylene plates and kept at 4 ± 1 °C for
maize    28.83    28.83    28.83 further analysis (11  days). The water activity (aw),
wheat    20.24    20.24    20.24 pH value and colour parameters (L*, a*, b*) of the
barley     4.96     4.96     4.96 samples were determined on days 1, 4, 7  and 11.
soybean meal, 48% CP    33.35    33.35    33.35 The water activity (aw) value was determined by an
sunflower meal, 28% CP    10.00    10.00    10.00 Aqualab 4TE device (METER Group, Inc., Pullman,
limestone2     1.37     1.36     1.35
WA, USA). A small amount of meat was placed in
dicalcium phosphate     0.65     0.65     0.65
the container of the device and the aw value was ob-
vitamin-mineral mix3     0.25     0.25     0.25
tained. The pH values of the samples were obtained
salt     0.24     0.24     0.24
according to the method reported by Gökalp et al.
L-lysine, hydrochloride     0.12     0.12     0.12
(2001). Accordingly, 10 g of homogenized samples
hesperidin4    0     0.1     0.2
Nutrient content, calculated
was weighed in parallel and 100  ml of pure water
dry matter, %    90    90    90
was added. After homogenizing with an Ultra-Tur-
crude protein (CP), %   23   23   23 rax device (T25, IKA Werk, Staufen, Germany) for
metabolic energy, kcal/kg 3000 3000 3000 1 min, pH values were determined using a pH-meter
calcium, %     0.80     0.80     0.80 (WTW Inolab, Weilheim, Germany). The sectional
usable phosphorus, %     0.30     0.30     0.30 surface colour densities of the samples (L*, a*, b*)
1
  Diets: C  – basal diet, HES1  – basal diet with 1 g/kg hesperidin, were determined using a Minolta colorimeter device
HES2 – basal diet with 2 g/kg hesperidin; 2 hesperidin replaced lime- (CR-200, Minolta Co, Osaka, Japan).
stone in the same amount in the groups with hesperidin addition;
3 
contained per kg: mg: retinol (vitamin A) 3, tocopherol (vitamin E) Lipid peroxidation analysis
30, menadione (vitamin K3) 5, thiamine (vitamin B1) 1, riboflavin (vita- In order to carry out the thiobarbituric acid reac-
min B2) 5, pyridoxin (vitamin B6) 3, nicotinic acid 30, pantothenic acid
10, folic acid 0.8, ascorbic acid (vitamin C) 10, choline chloride 450,
tive substances (TBARS) assay, in which malondi-
Co 0.2, I 0.5, Se 0.3, Fe 25, Mn 120, Cu 10, Zn 100; μg: cholecalciferol aldehyde (MDA) present in the sample is measured,
(vitamin D3) 62.5, cobalamin (vitamin B12) 20, biotin 100; 4 molecule for- the homogeneous samples of meat (about 2 g) were
mula: (C28H34O15), cas no: 520-26-13, purity grade 91% (Chem-Impex, homogenized with 12 ml of trichloroacetic acid
Wood Dale, IL, USA)
(TCA) solution (7.5% TCA, 0.1% EDTA, 0.1% pro-
pyl gallate (dissolved in 3 ml of ethanol)) for 15–20 s
Determining the performance values in an Ultra-Turrax device (T25, IKA Werk, Staufen,
The birds were weighed at the beginning of Germany) and then filtered through Whatman 1 fil-
the experiment and the beginning of fattening was ter paper. Filtrate (3 ml) was transferred to the test
determined by live weight. Then, the birds and the tube, and 3 ml of thiobarbituric acid (TBA) (0.02 M)
feeds were weighed on days 7, 14, 21, 28 and 35. solution was added and then it was homogenized
At the end of the experiment, each repetition was again. Next, the test tubes were kept in a water bath
weighed and divided by number of birds to obtain for 40 min at 100 °C and then cooled in cold water
the repetition average than the obtained values were for 5 min. After centrifugation (5 min at 2000 g), the
used to calculate the group average final live weight. absorbance values of the obtained liquid phase were
At the end of the experiment, total feed consumption obtained with use of a spectrophotometer (AquaMate
was calculated after subtracting the given feeds from 7000 Vis Spectrophotometer, Thermo Fisher Scien-
the remaining feeds. The feed conversion ratio (FCR) tific, Waltham, MA, USA) at 530 nm.
was calculated by dividing total feed consumed
Microbial analysis
throughout the experiment by the difference between
the final and initial live weights (weight gain). At the Microbiological analysis of the samples was
end of the experiment, 20 quails (12 for meat quality performed according to the proposed method by
and 8 for fatty acid analysis) from each group were Baumgart et al. (2015). Samples (25 g) of thigh meat
slaughted and the carcass weight was calculated after were homogenized in 225 ml of sterilized Ringer so-
removing the feathers, legs and internal organs post- lution. Then, the dilutions in Ringer solutions were
slaughter. Carcass yield was calculated by dividing prepared. The pouring method was used in the in-
the post-slaughter carcass weight by the final live oculations for all bacteria. The total number of me-
weight. sophilic aerobic bacteria (TMAB) was determined
370 Hesperidin addition to quail diets

on Plate Count Agar (PCA, Merck, Darmstadt, a rate of 4 °C/min, and held for 10 min. The device
Germany) medium. The petri dishes were incubat- was run at split mode, constant flow, 1 ml/min flow,
ed aerobically at 30 ± 1 °C for 72 ± 1 h. The total 20 ml/min of split and 1:20 of split ratio. The air was
number of psychotrophilic aerobic bacteria (TPAB) used at flow 350 ml/min and hydrogen – 35 ml/min.
was determined on PCA medium. The petri dishes The temperature of flame ionization detector (FID)
were incubated aerobically at 7 ± 1 °C for 10 days. was 260 °C (Thermo AI 1310, Thermo Fisher Scien-
The inoculation was performed by transferring 1 ml tific, Waltham, MA, USA). FAME mix (37C) stan-
from the suitable dilutions with coliform counts into dard solution (CL.40.13093.0001) in dichlorometh-
VRBA (Violet Red Bile Agar, Merck, Darmstadt, ane (Chem-Lab, Zedelgem, Belgium) was used for
Germany) medium. Petri plates were incubated in the identification of peak. Helium was used as the
anaerobic conditions for 2 days at 30 °C. The Mi- carrier gas. Fatty acid identification was performed
crococcus/Staphylococcus count was determined by comparing and calculating the standard fatty acid
on Mannitol Salt Agar (MSA, Merck, Darmstadt, peaks in the samples according to retention time
Germany) medium. The petri dishes were incubated using the Xcalibur program (Kramer et al., 1997).
aerobically at 30 ± 1 °C for 48 ± 1 h. The Lactoba- Saturated fatty acids (SFA), unsaturated fatty acids
cillus spp. count was determined on MRS (de Man, (UFA), polyunsaturated fatty acids (PUFA), mono-
Rogosa and Sharpe) Agar Base (Merck, Darmstadt, unsaturated fatty acids (MUFA), medium-chain
Germany) medium. The petri dishes were incubated fatty acids (MCFA) (fatty acids with chains contain-
anaerobically at 37 ± 1 °C for 72 ± 1 h. The Lac- ing from 6 to 12 atoms of C), long-chain fatty acids
tococcus spp. count was determined on M17 Agar (LCFA) (fatty acids with chains containing from
Base (Merck, Darmstadt, Germany) medium. The 14 to 20 atoms of C) and very long-chain fatty acids
petri dishes were incubated aerobically at 37 ± 1 °C (VLCFA) (fatty acids with chains containing above
for 38 ± 1 h. The obtained bacterial numbers were 20 atoms of C) were detected.
expressed as log CFU/g.
Statistical analysis
Fatty acid analysis The data obtained were evaluated using the
The meat samples were homogenized with tissue SPSS 20.0 statistical package programme (IBM
grinder (Homogenizer HS-30E, witeg Labortechnik Corp., Armonk, NY, USA). A one-way analysis of
GmbH, Wertheim, Germany) using a pestle with variance (ANOVA) was conducted in order to de-
polytetrafluoroethylene head (5553855 number, wi- termine whether there was a  statistical difference
teg Labortechnik GmbH, Wertheim, Germany). The between all parameters and the relevant data, and
grinded sample was mixed with 0.7 ml of potassium a  Bonferroni multiple comparison test was per-
hydroxide (10 M) and 5.3 ml of methanol and then formed for binary comparisons between groups
it was incubated at 55 °C for 45 min in an incuba- (P < 0.05).
tor (Nüve FN 120, Ankara, Turkey). The 0.58 ml of
H2SO4 (10 M) was added to the mixture, vortexed
and incubated at 55 °C for 45 min again. Then 3 ml of
Results
n-hexane was added to the mixture and the tubes It was observed that within the growth perfor-
were centrifuged at 1600 g for 5 min (Nüve, Anka- mance parameters, the initial and final live weights,
ra, Turkey) (Wang et al., 2015). After centrifugation, feed consumption, weight gain, feed conversion ra-
1.5 ml of supernatant was put into polytetrafluoreth- tio, carcass weight and yield were statistically simi-
ylene (PTFE)/ white silicone septa blue cap vials and lar in all groups (P > 0.05) (Table 2).
then analyzed in a gas chromatography device (Ther- The water activity of quail meat was found to
mo 1300, Thermo Fisher Scientific, Waltham, MA, be statistically similar in all groups regardless of
USA) with an automatic sampler (Thermo AI 1310, storage period (P > 0.05). Also there was no differ-
Thermo Fisher Scientific, Waltham, MA, USA). In ence between dietary groups in colour parameters
the analysis, a column of Fatty Acid Methyl Esters (L*, a*, b*) on days 1, 7 and 11, and in pH on days
(FAME) (TR-FAME, cat no: P/N 260M154P, Ther- 7 and 11 (P > 0.05). However, a statistical difference
mo Fisher Scientific, Waltham, MA, USA) (length: was observed between the dietary groups in terms
60 m, I.D.: 0.25 mm, film: 0.25 µm, and maximum of the L* (with the highest value in HES2 group),
temperature of 250/260 °C) was used. The initial a* (with the lowest value in HES2 group) and
temperature of the column was 100 °C, where it was b* (with the lowest value in HES1 group) values on
held for 3 min, and then it was rise to 240 °C at day 4 and the pH parameter on days 1 and 4 (P < 0.05).
A. Özbilgin et al. 371

Table 2. Effect of hesperidin addition in different doses to quail diets on growth performance parameters (n = 100; mean ± standard error)
Diet1
Indices P-value
C HES1 HES2
Initial body weight, g   45.39 ± 3.12   44.14 ± 0.63   42.95 ± 2.64 0.40
Final body weight (day 35), g 223.32 ± 3.92 222.48 ± 7.10 225.25 ± 1.97 0.92
Body weight gain, g 177.92 ± 2.83 178.34 ± 7.17 182.31 ± 1.33 0.76
Total feed consumption, g 565.64 ± 2.96 559.86 ± 10.92 569.94 ± 3.27 0.59
Average feed comsumption, g   42.88 ± 1.89   40.78 ± 2.64   41.98 ± 0.79 0.58
Feed conversion ratio, g/g    3.18 ± 0.47    3.15 ± 0.71    3.13 ± 0.20 0.74
Carcass weight, g (n = 20) 157.18 ± 3.85 160.32 ± 4.23 158.21 ± 3.82 0.85
Carcass yield, % (n = 20)   70.45 ± 1.23   74.00 ± 1.01   70.25 ± 0.60 0.31
1 
Diets: C – basal diet, HES1 – basal diet with 1 g/kg hesperidin, HES2 – basal diet with 2 g/kg hesperidin

On day 1, the pH was the highest in HES1 group TMAB (on days 1 and 11), Lactobacillus spp. (on
and the lowest in HES2 group, whereas on day 4 the days 1, 7 and 11), Micrococcus/Staphylococcus (on
pH value was the highest in HES1 group and groups day 4) and TPAB (on day 1 and 4), there was a sta-
HES2 and C did not differ (Table 3). tistically significant difference between the dietary
Lipid peroxidation in meat, measured as TBARS groups (P  < 0.05) (Table 4). TMAB was the high-
level, was decreased in HES1 and HES2 groups on est in HES2 group on day 1 and in C group on day
days 1 and 4 (P < 0.05). No such differences were 11. Lactobacillus spp. was the most abundant in meat
observed on days 7 and 11 (P > 0.05) (Figure 1). from HES2 group on day 1 and HES1 group on day 7.

Table 3. The effects of storage time and diet on some meat parameters of quails fed diets supplemented with different doses of hesperidin
(n = 12)
Storage times, days
Indices Diets1 P-value
1 4 7 11
pH C   6.15 ± 0.04b   6.27 ± 0.03b   6.36 ± 0.12   6.37 ± 0.03 0.12
HES1   6.26 ± 0.02aB   6.66 ± 0.06aA   6.29 ± 0.06B   6.30 ± 0.06B 0.001
HES2   6.02 ± 0.04cB   6.19 ± 0.05bAB   6.12 ± 0.05AB   6.26 ± 0.01A 0.01
P-value   0.001   0.001   0.600   0.210
L* C 44.34 ± 1.43 43.35 ± 1.32b 44.10 ± 0.61 45.73 ± 0.94 0.53
HES1 44.65 ± 0.84 39.24 ± 0.44b 43.41 ± 2.62 42.39 ± 2.43 0.25
HES2 45.78 ± 1.41 51.17 ± 1.85a 47.51 ± 3.28 45.93 ± 0.62 0.26
P-value   0.7100   0.000   0.480   0.240
a* C 10.87 ± 0.61 12.07 ± 0.98a 11.58 ± 0.25 10.93 ± 0.76 0.59
HES1   9.37 ± 0.38C 14.11 ± 0.70aA 10.77 ± 0.79BC 11.73 ± 0.88B 0.004
HES2 10.57 ± 0.66   8.01 ± 0.69b   9.56 ± 0.61 10.11 ± 1.11 0.17
P-value   0.190   0.001   0.100   0.490
b* C   7.99 ± 1.31   9.12 ± 0.67a   8.97 ± 0.92   7.54 ± 0.47 0.56
HES1   4.82 ± 0.70   6.02 ± 0.80b   6.37 ± 0.45   6.27 ± 0.25 0.27
HES2   7.80 ± 0.66   9.80 ± 0.82a   8.82 ± 0.83   5.63 ± 1.52 0.07
P-value   0.070   0.020   0.070   0.370
aw C   0.99 ± 0.001   0.99 ± 0.003   0.99 ± 0.002   0.99 ± 0.002 0.84
HES1   0.99 ± 0.004   0.99 ± 0.002   0.99 ± 0.002   0.99 ± 0.001 0.83
HES2   0.99 ± 0.002   0.99 ± 0.002   0.99 ± 0.001   0.99 ± 0.001 0.40
P-value   0.870   0.390   0.280   0.820
Diets: C – basal diet, HES1 – basal diet with 1 g/kg hesperidin, HES2 – basal diet with 2 g/kg hesperidin; L* – brightness, a* – redness,
1 

b* – yellowness, aw – water activity; a-c – means with different superscripts in the same column are significantly different at P < 0.05; A-C – means
with different superscripts in the same row are significantly different at P < 0.05

In terms of bacterial load in meat, Enterobac- Micrococcus/Staphylococcus ratio value was the
tericea and Lactococcus spp. counts were statisti- highest in HES2 group on day 4. Whereas TPAB
cally similar in the experimental groups in all stor- were the most abundant in both hesperidin groups
age time points (P  > 0.05). However, in terms of on day 1 and in HES2 group on day 4.
372 Hesperidin addition to quail diets

16

TBARS level, μmol malonaldehyde/kg

14 C HES1 HES2
12
10 a
a b c
8 b b
6
4
2
0
1 4 7 11
storage time, days

Figure 1. Effect of diet and storage time on TBARS level in meat of quails fed diets supplemented with different doses of hesperidin
Diets: C – basal diet, HES1 – basal diet with 1 g/kg hesperidin, HES2 – basal diet with 2 g/kg hesperidin; TBARS – thiobarbituric acid reactive
substances; a-c – bars with different letters within each storage time are significantly different at P < 0.05

Table 4. Effect of storage time and diet on some bacterial counts in meat of quails fed diets supplemented with different doses of hesperidin
(log CFU/g), (n = 12)
Storage times, days
Indices Diets1 P-value
1 4 7 11
TMAB C 2.99 ± 0.00bD 4.63 ± 0.33C 6.29 ± 0.21B 7.82 ± 0.03aA 0.001
HES1 3.56 ± 0.15bD 4.63 ± 0.35C 6.41 ± 0.15B 7.51 ± 0.10bA 0.001
HES2 4.52 ± 0.27aC 4.38 ± 0.08C 6.46 ± 0.05B 7.43 ± 0.00bA 0.001
P-value 0.020 0.790 0.730 0.040  
Enterobacteriacea C 1.95 ± 0.00B 1.95 ± 0.00B 2.80 ± 0.10A 3.15 ± 0.16A 0.002
HES1 1.85 ± 0.15C 2.23 ± 0.00BC 2.52 ± 0.04B 3.02 ± 0.17A 0.009
HES2 1.88 ± 0.10 2.56 ± 0.29 3.20 ± 0.50 3.45 ± 0.25 0.080
P-value 0.790 0.160 0.380 0.390  
Lactobacillus spp. C 3.10 ± 0.10cC 4.01 ± 0.12B 4.16 ± 0.16bB 4.68 ± 0.10bA 0.003
HES1 4.06 ± 0.02bD 4.38 ± 0.03C 4.90 ± 0.08aB 5.75 ± 0.11aA 0.001
HES2 4.67 ± 0.18a 4.06 ± 0.58 4.22 ± 0.04b 5.16 ± 0.15b 0.200
P-value 0.006 0.740 0.030 0.020  
Lactococcus spp. C 2.50 ± 0.20C 3.57 ± 0.14B 4.10 ± 0.06A 4.33 ± 0.05A 0.002
HES1 3.36 ± 0.37 4.23 ± 0.35 4.17 ± 0.07 4.70 ± 0.14 0.090
HES2 3.62 ± 0.32 3.74 ± 0.12 5.13 ± 0.37 4.90 ± 0.70 0.140
P-value 0.150 0.250 0.070 0.650  
Micrococcus/ C 2.95 ± 0.05C 3.90 ± 0.06bB 4.05 ± 0.05AB 4.15 ± 0.00A 0.001
Staphylococcus HES1 3.71 ± 0.10C 3.90 ± 0.01bB 3.96 ± 0.04B 4.18 ± 0.04A 0.001
HES2 3.96 ± 0.36 4.16 ± 0.04a 4.78 ± 0.44 3.74 ± 0.27 0.250
P-value 0.090 0.030 0.190 0.230  
TPAB C 1.34 ± 0.09bB 2.56 ± 0.08cB 5.30 ± 0.61A 6.05 ± 0.16A 0.001
HES1 3.11 ± 0.17aC 3.44 ± 0.02bC 4.66 ± 0.03B 5.57 ± 0.06A 0.001
HES2 3.09 ± 0.48aB 3.97 ± 0.09aB 5.69 ± 0.03A 6.34 ± 0.34A 0.005
P-value 0.040 0.002 0.260 0.180  
Diets: C – basal diet, HES1 – basal diet with 1 g/kg hesperidin, HES2 – basal diet with 2 g/kg hesperidin; TMAB – total mesophilic aerobic
1 

bacteria count, TPAB – total psychrophilic bacteria count; a-c – means with different superscripts in the same column are significantly different at
P < 0.05; A-D – means with different superscripts in the same row are significantly different at P < 0.05

A statistically significant difference was found (C20:0) content was the highest in HES2 group but
in the fatty acid profile between the experimen- there was no difference between HES2 and HES1
tal groups (P < 0.05) (Table 5). The content of groups; while lignoceric acid (C24:0) content was
γ-linolenic acid (C18:3n6) was decreased in HES2 the greatest in C group. There was also a  differ-
group whereas the content of α-linolenic acid ence between dietary groups in terms of the sum of
(C18:3n3), eicosapentaenoic acid (C20:5n3) doco- MCFA with the lowest value in HES1 group and the
sahexaenoic acid (C22:6n3) and the sum of n-3 fatty highest in C group, but with group HES2 not differ-
acids were in this group the highest. Eicosanoic acid ent either from group C or from group HES1.
A. Özbilgin et al. 373

Table 5. Effect of hesperidin addition into diet on fatty acid profile of thigh meat of quail, g/100 g (n = 8; mean ± standard error)
Diets1
Indices P-value
C HES1 HES2
Capric acid (C10:0)   0.02 ± 0.001   0.02 ± 0.001   0.03 ± 0.01 0.17
Lauric acid (C12:0)   0.12 ± 0.01   0.09 ± 0.001   0.11 ± 0.01 0.06
Myristic acid (C14:0)   0.67 ± 0.05   0.62 ± 0.003   0.67 ± 0.06 0.68
Myristoleic acid (C14:1)   0.18 ± 0.02   0.14 ± 0.01   0.22 ± 0.04 0.11
Pentadecanoic acid (C15:0)   0.10 ± 0.01   0.09 ± 0.001   0.19 ± 0.10 0.34
Palmitic acid (C16:0) 16.99 ± 0.43 18.84 ± 0.47 16.29 ± 1.89 0.29
Palmitoleic acid (C16:1)   6.51 ± 0.43   6.92 ± 0.56   7.12 ± 1.14 0.85
Heptadecanoic acid (C17:0)   0.20 ± 0.02   0.15 ± 0.01   0.18 ± 0.05 0.09
Stearic acid (C18:0)   4.06 ± 0.23   5.30 ± 0.25   7.47 ± 2.47 0.26
Oleic acid (C18:1n9) 34.76 ± 1.11 35.87 ± 0.80 34.20 ± 1.16 0.52
Linoleic acid (C18:2n6) 31.52 ± 0.78 28.44 ± 0.84 26.69 ± 3.15 0.23
α-linolenic acid (C18:3n3)   0.10 ± 0.02b   0.17 ± 0.01ab   1.18 ± 0.03a 0.001
γ-linolenic acid (C18:3n6)   1.45 ± 0.08a   1.33 ± 0.05a   0.91 ± 0.01b 0.01
Eicosanoic acid (C20:0)   0.05 ± 0.02b   0.07 ± 0.01ab   0.10 ± 0.01a 0.04
Eicosaenoic acid (C20:1)   0.01 ± 0.01b   0.03 ± 0.01a   0.03 ± 0.001ab 0.03
Arachidonic acid (C20:4n6)   1.41 ± 0.29   1.22 ± 0.24   2.23 ± 0.35 0.06
Eicosapentaenoic acid (C20:5n3)   0.06 ± 0.02b   0.08 ± 0.02b   0.16 ± 0.02a 0.007
Heneicosanoic acid (C21:0)   0.04 ± 0.01   0.05 ± 0.001   0.06 ± 0.01 0.25
Beheric acid (C22:0)   0.39 ± 0.15   0.17 ± 0.04   0.20 ± 0.06 0.21
Docosahexaenoic acid (C22:6n3)   0.28 ± 0.06b   0.40 ± 0.09b   0.88 ± 0.15a 0.001
Lignoceric acid (C24:0)   0.78 ± 0.17a   0.20 ± 0.03b   0.09 ± 0.07b 0.001
ΣSFA 23.12 ± 0.51 25.48 ± 0.66 26.04 ± 1.48 0.11
ΣUFA 76.89 ± 0.51 74.51 ± 0.66 73.89 ± 1.54 0.11
ΣMUFA 41.60 ± 1.13 43.03 ± 0.97 42.60 ± 1.47 0.69
ΣPUFA 35.29 ± 0.96 31.48 ± 0.87 31.29 ± 2.64 0.20
Σn-3   0.42 ± 0.06b   0.66 ± 0.11b   1.42 ± 0.11a 0.001
Σn-6 34.47 ± 0.94 30.65 ± 0.85 29.38 ± 3.16 0.19
Σn-9 41.51 ± 1.14 42.97 ± 0.96 42.17 ± 1.26 0.66
n-3/n-6   0.01 ± 0.001   0.02 ± 0.001   0.11 ± 0.08 0.24
MCFA   0.16 ± 0.02a   0.10 ± 0.01b   0.15 ± 0.01ab 0.02
LCFA 98.31 ± 0.24 99.00 ± 0.08 97.46 ± 1.21 0.33
VLCFA   1.54 ± 0.23   0.89 ± 0.08   2.33 ± 1.13 0.33
1 
Diets: C – basal diet, HES1 – basal diet with 1 g/kg hesperidin, HES2 – basal diet with 2 g/kg hesperidin; ΣSFA – total saturated fatty acids,
ΣUFA – total unsaturated fatty acids, ΣMUFA – total monounsaturated fatty acids, ΣPUFA – total polyunsaturated fatty acids, Σn-3 – total omega
3 fatty acids, Σn-6 – total omega 6 fatty acids, Σn-9  – total omega 9 fatty acids, n-3/n-6 – ratio of omega-3 and omega-6 fatty acids, MCFA –
medium-chain fatty acids, LCFA – long-chain fatty acids, VLCFA – very long-chain fatty acids; a-c – means with different superscripts in the same
row are significantly different at P < 0.05

Discussion weight increase and feed conversion ratio after

adding flavonoids to animal diets (Kamboh and Zhu,
Flavonoids are polyphenolic compounds that, 2013; Goliomytis et al., 2014, 2015). The present
when added to the diet, have many properties that study showed no effect of hesperidin on any growth
improve the growth performance of farm animals and performance or carcass parameter. Previous studies
the quality of the resulting product. Previous studies have reported that also citrus pulp (at a dose up to
examined the effects of flavonoids under temperature 60  g/kg feed) containing naringin (0.75–1.5  g/kg
stress on growth performance in animals (Kamboh feed), hesperidin (0.75–3.0  g/kg feed), quercetin
and Zhu, 2013). The present study examined the (0.5–1 g/kg feed) and flavanone did not affect growth
effects of the hesperidin flavonoid addition to quail performance when added to poultry rations (Simitzis
diets on the birds’ growth performance, physical and et al., 2011; Hajati et al., 2012; Goliomytis et al., 2014,
microbial quality of the carcass and the meat fatty 2015). It was also observed that Gingko biloba leaves
acid profile under normal temperature conditions containing high proportions of quercetin glycosides
Fattening performance. Varying results have (3.5 and 7 g/kg feed) (Cao et al., 2012) and quercetin
been obtained regarding feed consumption, live and citrus (0.25–1 g/kg feed) containing rutin active
374 Hesperidin addition to quail diets

ingredients (Peña et al., 2008) had no effect on live the present study, Nasr et al. (2017) found that meat
weight gain, feed consumption or FCR in broilers. pH values were between 6.11–6.28 in quails that
However, when hesperidin was added to the diet consumed the same diet but were classified accord-
at much lower rates (0.02  g/kg feed), it increased ing to feather colour. Simitzis et al. (2011) observed
the 42-day live weight of broilers and reduced the that the pH values of the meat at the 24th  hour of
FCR value (Kamboh and Zhu, 2013). Moreover, storgae were between 6.01–6.04 for broilers fed with
Sohaib et al. (2015) reported that supplementation hesperidin-supplemented (1.5 or 3 g/kg feed) diets.
of quercetin along with α-tocopherol (0.1–0.3 g/kg Leusink et al. (2010) reported that the pH value of
feed) caused an increase in growth performance and broiler breast meat did not change for broiler, fed
a decrease in FCR in broilers. In addition, Ouyang diets with different doses of cranberry fruit extract
et al. (2016) reported that adding alfalfa extracted (0, 40, 80 or 160  g/kg feed) and were 6.39, 6.37,
flavonoids (15  mg/kg feed) to broilers diets had 6.37 and 6.41, respectively. Genchev et al. (2008)
positive effects on daily live weight increase and observed that the pH value of quail meat was 6.17 at
FCR. The carcass yield for the C, HES1 and HES2 the 24th hour of storage and 6.47 on the 7th day. Kim
groups were 70.45, 74.0 and 70.23%, respectively. et al. (2020) reported that the pH value for the broil-
Although there was no significant difference between er meat on days 1, 3, 5, 7 and 9 was initially 5.95,
groups, it is noteworthy that the carcass yield was while it was 6.34 on the last day. However, in some
higher in the group with the low hesperidin dose studies, lower pH values than in the present study
(1 g/kg feed). The present study is consistent with were reported in meat samples. Goliomytis et al.
the previous studies. Caron et al. (1990) reported that (2015) reported a similar pH of 5.40 for the hesperi-
the carcass yield for 45-day-old quail was 67–70%. din, naringin and vitamin E supplemented and non-
The carcass yield of Japanese quails is determined supplemented poultry groups at the 24th hour of stor-
by the type, sex and slaughter age (Genchev et al., age. Peña et al. (2008) reported an average pH value
2008). The higher carcass yield of Japanese quails of 5.40 at the 24th hour for the meat of poultry which
is an indication of their superior productivity and consumed diets supplemented with flavonoids, such
ability to produce meat. as ascorbic acid, rutin and quercetin. Simitzis et al.
pH and colour parameters. When an animal is (2014) observed a pH value of 5.53 at the 24th hour
alive, the meat pH is around 7.3, while it drops down for hares consuming hesperidin-supplemented diets
to about 7.0 after slaughter and blood extraction. (1 and 2 g/kg feed). In these previous studies, it was
Lactic acid level increases because of a decrease in thought that there is a decrease in pH value due to
oxygen level and anaerobic glycolysis in the mus- the use of substances such as ascorbic acid as a sup-
cles after slaughter and this leads to a decrease in the plement to flavonoids.
pH value of the meat. The pH value of meat drops The colour of the meat is an organoleptic pa-
to 5.6–6.2 one hour after slaughter (Savell et al., rameter that is judged by consumers when shopping
2005). High meat acidity is considered as a sign of (Fanatico et al., 2007). Brightness (L*), redness (a*)
meat degradation caused by bacteria multiplication. and yellowness (b*) values are the basic measured
Researchers have reported that pH value should paramters of meat colour despite species (Uğurlu
decrease to 5.7–5.8 post rigor mortis (Savell et al., et al., 2017). In the present study, it was determined
2005; Jałosińska and Wilczak, 2009). However, un- that the colour parameters in quail meat were af-
like other poultry species (chicken and duck), the fected by the hesperidin addition but only on day
pectoral muscle in quails is not entirely glycolytic 7 of storage. At this time point, the higher dose of
but consists of dark muscle fibrils that prevent oxi- hesperidin increased brightness with a simultane-
dation. This explains the high pH in quail species ous decrease in redness; whereas yellowness was
compared to broilers. Pectoral muscle is the type of lower in the group fed with a lower dose of hesperi-
muscle in which post-slaughter rigor mortis occurs din. The average values of meat colour parameters
more slowly in quails (Drbohlav and Drbohlavova, in the present study were 44.8, 10.8 and 7.43, re-
1987; Riegel et al., 2003; Genchev et al., 2008). spectively for L*, a* and b*. Nasr et al. (2017) re-
In the present study, the pH values of the meat on ported that meat colour values of L* (44.23–46.40),
storage days 1, 4, 7 and 11 are observed to be be- a* (9.20–9.31) and b* (12.10–12.46) were de-
tween 6.02–6.66. Looking at pH values, in general, pendent on feather colours (white, yellow, black,
it was observed that the pH values of meat samples brown) in quails fed the same diet. However, a re-
from day 1 to day 11 did not change in HES1 group view of the literature shows a large discrepancy in
but increased in control and HES2 group. Similar to the results concerning the colour of poultry meat.
A. Özbilgin et al. 375

In comparison to the present study, Goliomytis et al.

    bacteria (TPAB), Enterobacteriaceae, Lactobacil-
(2015) found a more pronounced effect of hesperi- lus spp., Lactococcus spp. and Micrococcus/Staphy-
din at lower doses (0.75–1 g/kg) on the L*, a* and lococcus concentrations and storage time. Insausti
b* values for the breast meat of broilers. Simitzis et al. (2001) reported that 6–8 log CFU/g is an ac-
et al. (2014) reported that hesperidin (1–2 g/kg) in- ceptable microbial limit for the total number of bac-
fluenced to a greater extent L* and b* values and to teria in meat. Karayıldırım (2017) reported that hes-
a lesser extend a* value of breast meat of hares than peridin, when administered in vitro, has antibacterial
in the present study. Similarly, Riegel et al. (2004) activity on Gram-positive (Lactobacillus) and Gram-
obtained L*, a* and b* values of 40.0, 10.9 and 2.5, negative (Enterobacteriaceae) bacteria. The present
respectively, for turkey pectoral muscle 20 min af- study showed an increase for all bacterial species on
ter slaughter. In terms of L*, a* and b* values in day 11 of storage but any bacterial species exceeded
quail meat, Genchev et al. (2008) reported values of 8  log CFU/g. Previous studies reported results
40.81–45.67, 10.16–11.68 and 9.55–14.48 on days supporting the present study (Insausti, 2001; Nieto
1 and 7, respectively, which were rather similar to et al., 2012). Ambrosio et al. (2020) reported that cit-
values obtained in the present study. rus terpenes, when administered in vitro, had more
Lipid peroxidation. The most expected effect antibacterial activity on Escherichia coli (Gram-neg-
of flavonoids addition into diets is its influence on ative) than on Lactobacillus rhamnosus (Gram-pos-
lipid oxidation in meat. In the literature, flavonoid itive). In the present study, Enterobacteriaceae was
supplementation is reported to reduce MDA concen- stated as bacteria family with the lowest concentra-
tration (lipid peroxidation indicator) depending on tion at day 11. In the study supporting such a result,
storage time (Simitzis et al., 2011; Goliomytis et al., Nieto et al. (2012) were unable to detect Enterobac-
2014). In the present study, the concentrations of teriaceae bacteria, when they added thyme to lamb
MDA in thigh tissue of quails were lower in hesperi- rations at varying rates. However, in terms of total
din supplemented groups on days 1 and 4 of storage. bacteria, psychrophilic and lactic acid bacteria, the
Previous studies demonstrated a lower concentra- results of that experiment on day 11 were similar
tion of MDA in breast meat compared to thigh meat to the present study. Also, Kamboh et al. (2018) re-
(Goliomytis et al. 2014; Sohaib et al. 2015); how- ported that storing meat from poultry fed diets with
ever in the present study only the thight meat was genistein and hesperidin addition in the refrigerator
examined and it can be only stated that as a re- reduced microbial load of bacteria increasing deg-
sult of prolonged storage time (up to 11 days) radation parameters of meat and increased the total
MDA concentration increased with hesperidin amount of psychrophilic and lactic acid bacteria af-
effect in the first days of storage. Similar to the ter 15 days of storage. In the present study, psychro-
present study, the previous studies have pre- philic bacteria concentration increased upon storage
sented a decrease in the lipid peroxidation due to time both in the control and experimental groups.
supplementation of flavonoids (or extracts/ pulps Moreover, it was observed that hesperidin addition
containing them) such as quercetin (0.5–1  g/kg into quails diet increased psychrophilic bacteria con-
(Goliomytis et al., 2014) and 0.1–0.3 g/kg (Sohaib centration on days 1 and 4. However, especially the
et al., 2015)), naringin (0.75–1.5 g/kg; Goliomytis HES1 group (pH 6.30) among the hesperidin-sup-
et al. (2015)), hesperidin (1.5–3 g/kg; Simitzis plemented groups was observed to be more balanced
et al. (2011)), genistein and hesperidin (0.005  and than the C group, despite having a higher pH than the
0.02  g/kg, respectively; Kamboh and Zhu (2013)), C group (pH 6.40). In the same manner, as the pre-
isoflavones (0.01–0.08 g/kg; Jiang et al. (2007)), tea vious studies, it is thought that a lower degradation
catechins (0.05–0.3 g/kg; Tang et al. (2001)), grape occurs due to hesperidin supplementation compared
pulp (5–30  g/kg; Goñi et al. (2007); 15–60  g/kg; to storage time.
Brenes et al. (2008)) or Ginkgo biloba leaves (3.5 and Fatty acid profile. Saturated fatty acids (SFA),
7 g/kg; Cao et al. (2012)). especially stearic, lignoceric, palmitic and my-
Microbial load. One of the factors affecting ristic acids, are generally considered harmful to
meat quality is the microbial load of meat. Some health due to their hypercholesterolemic properties
microorganisms found in meat disrupt the quality (FAO/WHO, 2008). In the present study, hesperi-
of the meat, shorten its shelf life and pose a risk to din addition into quail diet did not influence the
human health. In such a  context, this study exam- sum of SFA as well as contents of the most com-
ined the relationship between total mesophilic aero- mon SFA such as lauric (C12:0), myristic (C14:0),
bic bacteria (TMAB), total psychrophilic aerobic palmitic (C16:0) and stearic (C18:0) acids. However,
376 Hesperidin addition to quail diets

eicosanoic acid (C20:0) content was the highest in (C20:4)) and total n-6 fatty acids. In the present
HES2 group but there was no difference between study, no effect of hesperidin on monounsaturated
HES2 and HES1 groups; while lignoceric acid fatty acids (MUFA) such as oleic and palmitoleic
(C24:0) content was the greatest in the control acid concentrations was stated.
group. The results of the present study match those
of Genchev et al. (2008) and Simitzis et al. (2014) Conclusions
regarding the composition of fatty acids in meat.
However, it does not match those of many previ- Hesperidin added to quail diets in varying doses
ous studies. Quercetin supplementation in lamb (1 and 2  g/kg) had a  limited effect on the growth
caused a decrease in SFA ratio (Andrés et al., 2014), performance parameters, such as live weight, feed
as well as fermented Ginkgo biloba leaves contain- consumption and feed conversion ratio. Neverthe-
ing flavonoids addition into broilers feed (Cao et al., less, it was determined that the hesperidin addition
2012). Kamboh and Zhu (2013) reported a decrease had an antibacterial effect on quail thigh meat and
in SFA upon supplementation of bioflavonoids in a  positive impact on lipid peroxidation and fatty
the ration, and an increase in the polyunsaturated acid profile of meat. So, it can be concluded that
fatty acid (PUFA) concentration. Besides PUFA the hesperidin addition to quail diets may both in-
content in meat was reported to be influenced by fluence shelf life quality of quail meat and exert
direct PUFA addition in the chicken diet (Cortinas a health-promoting effect increasing n-3 polyunsat-
et al., 2004). PUFA can be divided into n-3 (e.g., urated fatty acids content, which can increase con-
α-linolenic acid (C18:3), eicosapentaenoic acid sumer interest in quail meat.
(C20:5), docosahexaenoic acid (C22:6)) and n-6
(e.g., linoleic acid (C18:2), γ-linolenic acid (C18:3) Conflict of interest
and arachidonic acid (C20:4)). In the human diet,
n-3 and n-6 fatty acids have been reported to play an The authors declare that there is no conflict of
important role in the immune system due to being interest.
precursors to eicosanoids, prostaglandins, leukot-
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